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The Effects of Divided Attention During Encoding and Retrieval on Amnesic Patients' Memory Performance
THE EFFECTS OF DIVIDED ATTENTION DURING ENCODING AND RETRIEVAL ON AMNESIC PATIENTS’ MEMORY PERFORMANCE Laird S. Cermak and Bonnie M. Wong (Memory Disorders Research Center, Boston University School of Medicine, and Department of Veterans Affairs Medical Center, Boston)
ABSTRACT This study examined the effect of divided attention during encoding or retrieval on primary (recall) or secondary (button-pressing) task performance by amnesic patients and control subjects. Experiment 1 demonstrated that control subjects’ recall was affected by divided attention during encoding but not during retrieval, while the amnesic patients’ recall remained at the same low level for all conditions. Both groups showed a reduction in rate of buttonpressing during encoding relative to their baseline levels and a further reduction during the retrieval interval. In Experiment 2, five learning trials, instead of just one, were presented. This acted to increase all subjects’ recall and also had the effect of producing superior recall following free encoding relative to encoding during divided attention for the amnesic patients as well as for the control subjects. Button-pressing performance during the encoding interval increased to baseline for both groups during the five presentation trials, but there was no increase in the rate of button-pressing during the retrieval interval. Amnesic patients’ normal attention to the primary task during encoding and retrieval was felt to have several implications for future neuroimaging tasks with these patients. Key words: amnesia, divided attention, encoding, retrieval
INTRODUCTION Chronic amnesic patients tend to become a bit passive in their interactions with members of their families or with the activities going on around them on a ward. Their affect often becomes more reactive than proactive and their response to general questions becomes limited to single word replies. Of course, this is understandable given their situation in which a link to the past and future has become extremely fragile and they seem to retain only the ability to live in the moment. Withdrawal into passivity and general observation of the passing scene is a reasonable response to years of confusion and frustration, even when those years are essentially forgotten altogether. It seems that the amnesic patient has given up trying to remember in many cases. This being the general case for many amnesic patients, one has to wonder to what extent this affect carries over to their tendency to try to perform well on a wide variety of memory tasks given to them over the months and years since they became amnesic. They appear to be motivated and willing to test, but to what extent are they really engaged in the activity and at least attempting to do the task at which they are failing so miserably? Every investigator of the amnesic syndrome knows that the patients is going to fail their recall or recognition task, but still must harbor thoughts of Cortex, (1999) 35, 73-87
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how hard the patient is actually trying in the face of such long term failure. This would be especially true for those patients who are quite aware of their disability. We have often had patients exclaim to us during testing that “This is exactly the kind of thing I can’t do”. Knowledge of the extent of involvement by the patient during a memory task would be most relevant when one is considering the relative contribution of amnesic patients’ depressed encoding and inadequate retrieval capabilities to the determination of their overall memory deficit (Cermak, 1977; Warrington and Weiskrantz, 1978). The question which has always been of some concern without ever being given much voice is whether or not the amnesic patient expends the same amount of effort that a normal subject commits to translating material into a form amenable to retrieval or in applying search strategies during retrieval. The difficulties an amnesic patient has encoding the properties of tobe-remembered information may emanate as much from a lack of effort committed to the translation as from an inability to perform such a tranformation. It is also possible that the amnesic patient may actually have suffered as much from an unwillingness to try to expend sufficient cognitive effort required to search their memory for the desired response during retrieval as for an inability to locate that information. These two possibilities have probably not been explored for two reasons: First, the patients appear to be highly diligent and attentive during both encoding and retrieval even when their daily affect has become rather lethargic, and second, there is no direct means of assessing this level of resource allocation. Recently, however, a paradigm which focuses on the amount of effort subjects expend on a secondary task during encoding and retrieval of to-beremembered material has been introduced by Craik et al. (1996). The paradigm utilizes a divided attention task in which the subject is asked to perform a secondary, ongoing task while also engaging in an attempt to encode or retrieve words. While the paradigm does not directly measure the amount of effort expended on the primary tasks of encoding and retrieval, it does require that the subject at least “divide” his attentional resources in order to try to optimize performance on the two tasks. If our amnesic patients expend little effort toward encoding the information, then their rate of secondary task performance will not be affected relative to baseline performance on the secondary task. Likewise, if the patients totally abandon the search process during the retrieval interval, then their rate of responding on the secondary task will not suffer. However, if the patients expend any amount of effort trying to perform the primary tasks of encoding or retrieving, then the rate of responding on the secondary task would decline during that interval. Determining whether or not the amount of effort the patients expend on the primary tasks is the same as normal control subjects would be important to know for two reasons: First, it is imperative that we determine that amnesic patients are putting forth normal effort during the processes of encoding and retrieval search before we ascribe too much credence to the lack of “quality” of their processing during these two stages of information processing. Second, investigators need to know that the patients are exerting as much effort into these processes as are normal control subjects when documenting the on-line
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processing abilities of amnesic patients using neuroimaging techniques such PET or fMRI. If the amnesic patient is not attempting to encode a word on any cognitive level, or is not trying to search for an item in memory using some strategy, even if deficient, then differences seen in their fMRI might not reflect real qualitative differences in the integrity of a mnemonic process so much as lack of effort on that level. Meudell, Mayes and MacDonald (1994) have shown that resource allocation may be a problem for amnesic patients on nonmnemonic tasks, so it becomes essential that we determine whether or not amnesic patients exert normal effort, as defined by allocation of resources, during the encoding and retrieval of verbal information. In order to investigate this ability, we adapted the Craik et al. (1996) divided attention paradigm for use with amnesic patients. EXPERIMENT 1 Materials and Methods Subjects The participants in this experiment consisted of two groups of amnesic patients and two control subject groups. Amnesic Korsakoff Patients. The first group of amnesic patients consisted of 8 men diagnosed with alcoholic Korsakoff syndrome, all residing at various private care facilities in the greater Boston area. All of these patients had a severe anterograde memory defect, as assessed by both clinical presentation and an extensive memory battery given at the Memory Disorders Research Center (MDRC). Prior to testing, these patients were presented at Memory Rounds and diagnosis unanimously confirmed by attending neurologists, neuropsychologists and staff members of the MDRC. All of the patients were unable to recall any day to day events, could not learn the names of individuals doing the testing, were somewhat disoriented in time and space and had extensive retrograde amnesia of varying lengths all being essentially complete for episodic material. The mean age for this patient group was 65 years, with a mean education level of 11.4 years. On the Wechsler Adult Intelligence Scale-Revised (Wechsler, 1981), the mean Verbal IQ for this groups was 92. On the Wechsler Memory Scale-Revised (Wechsler, 1987), the average Attention/Concentration index was 99, General Memory index was 79.1, and Delayed Memory index was 57.5. This patient group received a full battery of neuropsychological tests prior to experiment participation at the Memory Disorders Research Center. The patients scored significantly below normal on the Warrington Recognition of Faces and Words Test, the Rey Auditory Verbal Learning Test (RAVLT), the California Verbal Learning Test (CVLT) and Continuous Visual Memory Test (CVMT), and on retrograde memory assessments using the Boston Famous Faces and Events, Crovitz Autobiographical Questionnaire, and the Transient Events Test. On non-memory neuropsychological tests, subjects in this patient group scored at or above normal on the Boston Naming Test (BNT), Boston Diagnostic Aphasia Examination (BDAE), American National Adult Reading Test (ANART), Wide Range Achievement Test (WRAT), Line Orientation, Face Recognition, and Drawing tasks. Mixed Etiology Amnesic Patients. The second group of amnesic patients consisted of 4 men and 4 women with amnesias of varying etiologies. All eight patients who presented with amnesias were as dense clinically on the MDRC memory battery as the Korsakoff patients described above. Four of these patients became amnesic following anoxic episodes due to: an asthma attack in on case, a drug overdose in another case, and a massive myocardial infarction in the remaining two cases. Two patients
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became amnesic after contracting encephalitis with damage to the medial temporal lobes; one patient suffered a bilateral thalamic stroke; and one patient sustained a subarachnoid hemorrhage secondary to an aneurysm. The mean age for this group was 53.6 years, with a mean education level of 15.3 years. The mean WAIS-R Verbal IQ for this patient group was 102.3. The average Attention/Concentration index on the WMS-R was 99.4, the average General Memory index was 79.8, and the average Delayed Memory index was 60.1. This group also scored significantly below normal on the Warrington Recognition of Faces and Words test, the RAVLT, the CVLT, the CVMT and on our battery of retrograde memory tests. They scored normally on the BNT, the BDAE, the ANART, the WRAT, Line Orientation, Face Recognition and Drawing tasks. Alcoholic Control Subjects. The control group for the Korsakoff patients consisted of 8 chronic alcoholic controls (6 men, 2 women) living in private homes in the Boston area. None of these subjects showed any signs of neurological or psychiatric illness. All had abstained from alcohol consumption for at least six months prior to testing. Subjects in this group were matched with the Korsakoff amnesic group according to age, WAIS-R Verbal IQ, and education. The mean age of this group was 59.9 years, with a mean education level of 12.8 years. The average WAIS-R Verbal IQ for this group was 96.3. The average Attention/Concentration index on the WMS-R was 97.3, the average General Memory index was 103.3, and the average Delayed Memory index was 98.1. Normal Control Subjects. The control group for the mixed etiology amnesic patients consisted of 6 men and 2 women who had no prior history of alcohol abuse, neurological illness, or psychiatric disorder. Subjects in this group were matched with the mixed etiology amnesic group according to age, WAIS-R Verbal IQ, and education. The mean age of this group was 57.5 years, with a mean education level of 13.9 years. The average WAIS-R Verbal IQ for this group was 104.4. All normal control subjects were living in private homes in the Boston area. Stimuli The stimuli used in this experiment were two-syllable common concrete nouns selected from the Toronto Word Pool (Friendly et al., 1982). Stimuli were selected based on their average concreteness (on a scale of 1 to 7), with all of the words averaging 6.0 or higher. The stimuli were divided into 8 lists of 15 words each. An individual subject received only four word lists in this experiment, but all eight lists were used across subjects in this task and each word list was equally represented in each condition for all groups. Three of the four word lists that were not used in this experiment were later utilized in the second experiment that is reported in this manuscript. Design This was a Divided Attention experiment in which the subjects performed both a memory task and a button-pressing task. The memory task consisted of the experimenter reading a 15-word list to the subject, at a rate of 4 seconds per word. The subjects were then asked to recall as many of these words as possible during a 60-second retrieval interval. The subjects’ responses were recorded by the experimenter as the number correct given during each of six, 10-second intervals of the 60-second retrieval phase. The button-pressing task required that subjects view a display on the screen of a Macintosh Powerbook (using Psychlab software) and respond using a three-button button box. The visual display consisted of a row of three boxes shown across the screen with an asterisk programmed to appear randomly in one of the three boxes. The subject’s task was to press the button on the button box which corresponded to the position of the asterisk (i.e., if the asterisk appeared in the center box, the subject pressed the center button on the button box). A correct response by the subject resulted in the asterisk moving to a different box. An incorrect response had to be corrected before the asterisk would move to another box. Subjects were asked to perform as quickly and as accurately as possible, using their
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preferred hand. The asterisk was programmed never to appear in the same box on successive trials. Each subject performed in four different experimental conditions with a different word list used for each condition. The conditions consisted of combinations of divided attention (button-pressing) during either encoding or retrieval, during neither interval, or during both. Each subject participated in a condition of divided attention during the time that the material was being presented (divided attention at encoding) and a condition where the material was presented without distraction (free encoding). Likewise, the subject also participated in two retrieval conditions, one with divided attention (divided attention at retrieval) and one without distraction (free retrieval). The four conditions can be thought of as: 1) No divided attention at either encoding or retrieval, essentially a baseline condition. 2) Divided attention only at encoding and not at retrieval, which we refer to later as DA@Enc. 3) Divided attention only at retrieval and not at encoding i.e., DA@Ret. 4) Divided attention at both encoding and retrieval, i.e. DA@Enc. and DA@Ret. in the same condition. The order of the four experimental conditions was partially counterbalanced so that occurrence of each condition appeared equally often as the first, second, third or fourth task attempted. Procedure Each subject was tested individually in a private room accompanied by an Experimenter who administered instructions, initiated the preprogrammed experiment and recorded correct responses during the retrieval interval. Before beginning the actual experiment, each subject performed the button-pressing task for 60 seconds as practice and to familiarize them with the procedure. Then, subjects received their first experimental condition. Following the completion of this task, each subject was again asked to perform the button-pressing task for 60 seconds to obtain a baseline index of the subject’s button-pressing during the procedure free from having to perform the primary task. Next, each subject received the second experimental condition, after which there was a five-minute rest break. At the end of the break, each subject received the third experimental condition, followed by another 60-second button-pressing task, and finally, their fourth experimental condition. Thus, subjects performed the button-pressing task alone a total of three times during the entire experiment. The reaction times from the latter two of these instances was used as a baseline measure of each subject’s average button-pressing rate.
Results The Korsakoff patients and the mixed etiology amnesic patients were combined into one Amnesic group when preliminary analyses revealed no significant differences in performance between the two groups. This was true both for the number of words recalled by condition and for the number of button presses during each phase of the experiment. The alcoholic control subjects and the normal control subjects were also combined into one Control group because there were no significant differences in performance between these two groups for words recalled and for the number of button presses. During the recall phase, words produced by subjects that matched the target words were counted as correct responses. During all phases of the experiment, the number of button presses was recorded for each ten-second interval. Word Recall The mean number of correctly recalled words following the two conditions introduced at encoding (Divided Attention at Encoding and Free Encoding) and the two conditions at retrieval (Divided Attention at Encoding and Free
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Encoding) is shown for each group in Table I. An overall 2 × 2 × 2 ANOVA was performed on these scores using Group (Amnesic, Control) as the betweensubjects factor and the Encoding Conditions (Free, Divided) and Retrieval Conditions (Free, Divided) as within-subject factors. This analysis revealed a significant difference between Groups, F (1, 30) = 44.59, p < .01; between Encoding Conditions, F (1, 30) = 23.72, p < .01; and between Retrieval Conditions, F (1, 30) = 16.04, p < .01. In addition, one interaction achieved significance: Group × Encoding, F (1, 30) = 10.70, p < .01. The Triple interaction was not significant. TABLE I
Experiment 1 – Mean Number of Correctly Recalled Words as a Function of the Encoding (Free, Divided) or Retrieval (Free, Divided) Condition Encoding
Controls Amnesics
Retrieval
Free
DA
Free
DA
6.47 3.38
4.72 3.03
6.09 3.62
5.09 2.78
Simple effects revealed that the amnesic patients recalled fewer items than the control subjects both for the Free Encoding and for the Divided Attention at Encoding Conditions (both p’s < .01). The amnesic patients failed to show any differences between Encoding Conditions, while the control subjects recalled more items in the Free Encoding Condition (p < .01) than in the Divided Attention at Encoding Condition. This improvement by the control subjects probably accounted for most of the significant Group × Retrieval Condition Interaction. The Amnesic patients also recalled fewer items than the control subjects for both the Free Retrieval and Divided Attention at Retrieval Conditions (both p’s < .01). Both groups recalled more items during Free Retrieval than during Divided (p’s < .01) with no difference in the pattern of retrieval as evidenced by a lack of significance in the Group × Retrieval Condition Interactions. Button-Press Responding The mean number of button presses produced by each group during the two divided attention phases of the experiment (Encoding and Retrieval) as well as at Baseline is shown in Figure 1. A Group (Amnesic, Control) × Condition (Baseline, Encoding, Retrieval) ANOVA revealed a significant difference between Groups, F (1, 30) = 6.14, p < .05 and a significant difference between Conditions, F (2, 60) = 159.30, p < .01. The interaction between Group and Conditions was not significant. Simple effects revealed that the rate of button pressing differed between groups at both Baseline and Encoding (p’s < .05) but not during Retrieval. Rate of button pressing was significantly greater during the Baseline Interval than during Encoding for both Groups and for the Encoding interval relative to Retrieval interval for both Groups as well (p’s < .01).
Mean number of button presses
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Baseline (controls) DA@Enc. (controls) DA@Ret. (controls) Baseline (Amnesics) DA@Enc. (Amnesics) DA@Ret. (Amnesics)
Time interval Fig. 1 – The mean number of button presses per ten second interval for each group at baseline, simultaneous with encoding and with retrieval during Experiment 1.
A 2 × 3 × 6 ANOVA was also performed using Time Interval (10, 20, 30, 40, 50 and 60 secs.) as a within-subject factor in order to determine whether the rate of responding was constant within a condition. This analysis revealed a significant difference between Groups, F (1, 30) = 6.17, p < .05; Conditions, F (2, 60) = 159.28, p < .01; and Time Intervals, F (5, 150) = 30.78, p < .01. No interactions with Group attained significance, but the Condition × Time Interval interaction was significant, F (10, 300) = 11.71, p < .01. As can be seen in Figure 1, this interaction was primarily determined by the reduced responding that occurred during the first thirty seconds of Retrieval. The rate of responding across the other two conditions was relatively constant for both groups. Discussion The amnesic patients, as would be expected, recalled fewer words than did the control subjects across all the conditions of this experiment. More importantly though, the pattern of these amnesic patients’ recall differed somewhat from that of the control subjects. The control subjects recalled significantly more words when their attention was not divided during encoding than when it was divided, whereas the amnesic patients’ recall did not improve when encoding was performed without the restrictions imposed by having to simultaneously perform the secondary, button-pressing task. The amnesic patients’ recalled approximately the same number of items when they were free to attend solely to the words they had to remember and when they had to divide their attention betweeen this task and the button-pressing task. It was as if the additional time and/or resources available for the single task of encoding were not utilized as effectively for the amnesics as it was for the control subjects.
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The pattern of recall during free and divided attention conditions at retrieval was the same for both the amnesic patients and the control subjects. Both groups recalled more words when attention was not divided at retrieval than when it was. Craik et al. (1996) had reported that divided attention at retrieval did not have any effect for college students (only divided attention at encoding seemed to change these subjects’ recall ability). However, we found that divided attention at retrieval was nearly as detrimental as at encoding for our older and alcoholic subjects. The college students seemed able to overcome the interference produced from having to perform the secondary task during retrieval to a far greater extent than did our older subjects. Comparing the rate of performance on the button-pressing task for the two groups in our experiment, we found that the amnesic group performed below the control group throughout the experiment. They made significantly fewer button presses during the Baseline period and during the Encoding interval. At Retrieval the difference was again present, but this difference did not attain significance (p < .10). The pattern of responding across conditions was, however, precisely the same for both groups. The number of button presses during Encoding was less than during the Baseline, and the number of bar presses at Retrieval was smaller still. This latter effect was largely produced by the first half of the retrieval period (see Figure 1), as the subjects tried hardest to recall, but was still apparent throughout the retrieval interval. Even during intervals where subjects failed to retrieve a single word, their rate of button pressing remained below baseline. This outcome suggests that the amnesic patients were at least still trying to search for the words. Likewise, during the encoding interval, it has to be concluded that the amnesic patient is at least attending to the words since they do slow down somewhat on the secondary task. This does not mean that the amnesic patients’ encoding or retrieval strategies necessarily parallel those of the controls but rather that they are not ignoring the primary task. Given the rather low recall performance of all the subjects on this task, we feared that both the pattern of recall and the pattern of button pressing may have been a function of the low level of actual output of words for these subjects during retrieval. Since the subjects had so little information available to them with which to work, it seemed possible that the effect of recalling words on the secondary task had been underestimated. If the subjects had had more trials to learn the words then at the time of retrieval they may have had more information available to them to retrieve, and this, in turn might have resulted in greater impairment in the button-pressing performance. Alternatively, it could be that with better learning, the control subjects might find retrieval easier, as we have hypothesized was the case for college students in the Craik et al. (1996) experiment, and would then be free to devote more resource to the secondary task. This would be reflected in superior button-pressing performance for the control subjects relative to the amnesic patients, a result that did not occur with the low levels of item acquisition evident in Experiment 1. We also felt that if we provided more learning trials during the encoding condition, we might find less effect on the secondary task during the encoding interval as
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learning trials progressed. If less attention had to be paid to the encoding task, then more effort could be expended on the button pressing. To test these assumptions, we proceeded to give subjects five learning trials prior to their retrieval interval. EXPERIMENT 2 Materials and Method Subjects Amnesic Patient Group. The amnesic patient group consisted of seven men diagnosed with alcoholic Korsakoff syndrome and seven amnesic subjects with varying etiologies (4 men, 3 women). The mean age for the Korsakoff group was 67 years, with a mean education level of 11.3 years. On the Wechsler Adult Intelligence Scale-Revised (Wechsler, 1981), the mean Verbal IQ for this group was 91.7. On the Wechsler Memory Scale-Revised (Wechsler, 1987), the average Attention/Concentration index was 99.3, the average General Memory index was 78.4, and the average Delayed Memory index was 58.7. The mean age of the mixed etiology amnesic group was 53.6 years, with a mean education level of 15.7 years. The mean WAIS-R Verbal IQ for this patient group was 102. The average Attention/Concentration index on the WMS-R was 98.1, the average General Memory index was 78.6, and the average Delayed Memory index was 58.6. Control Subject Group. The control group for the amnesic patients consisted of 7 chronic alcoholic subjects (6 men, 2 women) and 7 normal control subjects (4 men, 3 women). The mean age of the alcoholic control group was 62.6 years, with a mean education level of 12.3 years. The mean WAIS-R Verbal IQ for this group was 98. The average Attention/Concentration index on the WMS-R was 103.4, the average General Memory index was 104.9, and the average Delayed Memory index was 100.4. The mean age for the normal control group was 55.3 years, with a mean education level of 14 years. The mean WAIS-R Verbal IQ for this group was 106.1. All normal control subjects were living in private homes in the Boston area. Stimuli The stimuli used in this experiment came from the same two-syllable common concrete nouns selected from the Toronto Word Pool (Friendly et al., 1982) used in Experiment 1. Specifically, each subject received three of the eight 15-word lists that he or she had not received in Experiment 1. This resulted in the same word lists being re-presented in both experiments without any individual ever encountering the same list. The lists were counterbalanced across all three conditions in this experiment just as they had been in Experiment 1. Design The design was identical to the one used in Experiment 1, with two exceptions. The first difference was that the word lists were read to subjects five times in a row during the free encoding and divided encoding phases, rather than just once. The second difference was that the divided attention at both encoding and at retrieval condition was not utilized in this study. Thus, each subject performed in three, rather than four, experimental conditions with one of the three different word lists used in each condition. Subjects received a Free Encoding-Free Recall task (Baseline condition), a Divided Attention at Encoding-Free Recall task (DA@Enc.), and a Free Encoding-Divided Attention at Recall (DA@Ret.) task. Before beginning the experiment, subjects performed the button-pressing task for 60 seconds as practice to familiarize the subject with the task. Then, the subjects received one of the three experimental conditions.
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Procedure Both the memory task and the button-pressing task were identical to those performed by subjects in Experiment 1. Since many of the amnesic patients participated in Experiment 1, at least two months intervened between test sessions. None of the control subjects had participated in Experiment 1.
Results Word Recall As in Experiment 1, the Korsakoff patients and the mixed etiology amnesic patients were combined into one Amnesic group when preliminary analyses revealed no significant differences in performance between the two groups. Similarly, the alcoholic control subjects and the normal control subjects were combined into one Control group since there were no significant differences in performance between these two groups. Encoding: The mean number of words correctly recalled following Free Encoding or Divided Attention (DA) at Encoding is shown for each group in Table II. An overall ANOVA performed on these scores using Group (Amnesic, Control) as the between-subjects factor and Encoding Condition (Free, DA at Encoding) as the within-subject factor revealed a significant difference between TABLE II
Experiment 2 – Mean Number of Correctly Recalled Words as a Function of the Divided Attention (DA) Condition: No DA, at Encoding (DA at Encoding) and at retrieval (DA at Retrieval)
Controls Amnesics
No DA
DA at Encoding
DA at Retrieval
9.64 4.93
7.57 3.57
9.57 5.00
Groups, F (1, 26) = 21.60, p < .01 and between Conditions, F (1, 26) = 14.64, p < .01. The Group × Encoding Condition interaction was not significant. Simple effects revealed that the amnesic patients recalled fewer items than the control subjects following each Encoding Condition (p’s < .01). Across conditions, both the amnesic patients and the control subjects recalled more items in the Free Encoding than in the DA at Encoding Condition (p’s < .05). Retrieval: The mean number of words correctly recalled during Free Recall or Divided Attention at Retrieval is also shown for each group in Table II. An overall ANOVA performed on these scores using Group (Amnesic, Control) as the between-subjects factor and Retrieval Condition (Free, DA at Retrieval) as the within-subject factor revealed a significant difference between Groups, F (1, 26) = 29.65, p < .01 but absolutely no difference (they were equal) between Conditions. The Group × Retrieval Condition interaction was also not significant. Simple effects revealed that the amnesic patients recalled fewer items than the control subjects for each Retrieval Condition (p’s < .01), but neither group demonstrated any difference in recall between the Free Recall and the DA at Retrieval Conditions.
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Divided Attention at Encoding Contrasted with Divided Attention at Retrieval: Recall following Divided Attention at Encoding relative to recall following Divided Attention at Retrieval could be compared in this paradigm by performing a Groups (Amnesic, Control) × Conditions (Free Encoding and Retrieval, DA et Encoding, DA at Retrieval) ANOVA. This analysis revealed a significant difference between Groups, F (1, 26) = 30.42, p < .01 and between Conditions, F (2, 52) = 9.48, p < .01. The interaction was not significant. Simple effects showed that the Group difference occurred at every Condition (p’s < .01). In addition, both Groups showed significantly less recall following DA at Encoding than during DA at Retrieval (p’s < at least .05). The recall following DA at Retrieval was actually as good as the Free Encoding-Free Retrieval Condition. Button-Press Responding
Mean number of button presses
The mean number of button presses produced by each group during the two divided attention phases of the experiment (Encoding and Retrieval) as well as at Baseline is shown in Figure 2. A Group (Amnesic, Control) × Condition (Baseline, Encoding, Retrieval) ANOVA revealed no significant difference between Groups (there had been a significant difference in Experiment 1), but a significant difference between Conditions, F (2, 52) = 135.32, p < .01 (as had been the case in Experiment 1). The interaction between Group and Conditions was significant, F (2, 52) = 3.58, p < .05 (this interaction had not been significant in Experiment 1). The difference in the number of button presses was never significantly different between Groups at any point. Thus, it appears that the significance was produced by the consistently faster responding by the control subjects relative to the amnesic patients during both the Baseline and the
Baseline (controls) DA@Enc. (controls) DA@Ret. (controls) Baseline (Amnesics) DA@Enc. (Amnesics) DA@Ret. (Amnesics)
Time interval Fig. 2 – The mean number of button presses per ten second interval for each group at baseline, simultaneous with encoding and with retrieval during Experiment 2.
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Encoding intervals but slower responding by the control subjects than by the amnesic patients during the Divided Attention at Retrieval interval. Overall the rate of responding was significantly greater during Baseline and Encoding for both Groups relative to the Retrieval interval (p’s < .01). A 2 × 3 × 6 ANOVA was also performed using Time Interval (10, 20, 30, 40, 50 and 60 secs.) as a within-subject factor in order to determine whether the rate of responding was constant within a condition. This analysis revealed no significant difference between Groups, F (1, 26) = 0.38. There was, however, a significant difference between Conditions, F (2, 52) = 122.52, p < .01; and Time Intervals, F (5, 130) = 32.82, p < .01. Both of the interactions with Condition attained significance: Group × Condition, F (2, 52) = 4.63, p < .01 and Condition × Time Interval, F (10, 260) = 11.82, p < .01. No other interactions were significant. As can be seen in Figure 2, the interactions were primarily determined by the slower rate of responding in the Retrieval Condition during the early intervals. Furthermore, this outcome was primarily determined by the Control Group as demonstrated by the significant Group × Condition interaction. The rate of responding across the other two conditions was relatively constant and this pattern was the same for both groups. Discussion As in Experiment 1, the amnesic patients recalled fewer words overall than did the control subjects. However, in the present experiment each group displayed the same pattern of recall performance. Recall of words was worse following divided attention during encoding than it was following the free encoding condition. However, recall was not significantly different for either group when divided attention occurred during the retrieval task than when retrieval was free. Contrasting recall between divided encoding and divided retrieval conditions revealed that divided attention at encoding disrupted recall to a significantly greater extent than divided attention at retrieval for both groups. In fact, as just noted above, divided attention at retrieval produced no noticeable effect on recall; only divided attention at encoding had this deleterious effect. The button pressing task also produced somewhat different results than had been reported for Experiment 1. In the present experiment, the amnesic patients’ performance was quite similar to that of the control subjects. There was no overall difference between the two groups in the number of button presses that were made across the entire experiment and no single point at which performance differed significantly. Both groups responded essentially the same during Encoding as they had during Baseline but significantly below this level during the Retrieval task. However, the two groups did not retain their same relative relationship across all three conditions resulting in the significant Group × Condition interaction. While the amnesic patients’ Baseline and Encoding button press rates were always below that of the control subjects, the amnesic patients’ rate of button pressing during Retrieval was above that of the control subjects. Thus, even though both groups slowed their rate of button pressing
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during the Retrieval stage, the control subjects must have done so to a significantly greater extent. This effect of slowing for retrieval extended across all time intervals but it was greatest during the first 30 seconds. GENERAL DISCUSSION The absolute number of words that amnesic patients were able to recall changed very little between Experiments 1 and 2 even though the paradigm used in the second experiment included five learning trials while the first had only one. However, the “pattern” of their recall did shift. In Experiment 1, there was no difference in recall between free encoding and encoding in the face of distraction from the secondary task. In Experiment 2, the amnesic patients demonstrated better retrieval under conditions of free encoding than they did under conditions of divided attention. This effect seemed to be largely produced by the fact that the patients were able to increase their retention from one learning trial to five when attention was not divided but could not do so under conditions of divided attention. The control subjects, on the other hand, demonstrated superior retrieval with no distraction relative to recall following divided attention at encoding after just one learning trial and retained the same relative difference between conditions following five learning trials even though the level of recall increased dramatically for both conditions. A more dramatic effect on recall performance following five learning trials occurred on the retrieval side for both groups. Following five learning trials, recall ability under the condition of divided attention was as good as recall when no secondary task was present. Following one learning trail (Experiment 1), divided attention at retrieval had produced a disruptive effect on the participant’s ability to recall the material. Thus, we found for both groups that divided attention at retrieval seems to have an effect on recall ability only for “underlearned” material, but has little effect on recall once that material has had the opportunity to be more fully acquired. Of utmost interest, is that this was true for the amnesic patients as well as for the control subjects. Obviously the amnesic patients did not acquire as much information as the control subjects, but apparently whatever level of acquisition they did attain stood up well in the face of distraction. This effect of level of acquisition on immunity to the distraction produced by divided attention did not occur for the college students in the original Craik et al. (1996) study. Those subjects demonstrated no effect of divided attention during retrieval on recall performance even though they had had only one acquisition trial. Apparently their subjects required only one presentation to acquire the material adequately. But clearly this was not the case for our older, and in some cases alcoholic, subjects or for our amnesic patients. It seems that our older subjects took more than one trial to achieve their maximum potential so that divided attention at retrieval would no longer have any effect on their recall. The results for the rate of button pressing during encoding or retrieval showed almost the mirror effect of that just described for recall when the
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increase from one learning trial to five is considered. For both the amnesic patients and the control subjects the rate of button pressing was slower during retrieval than during encoding, but the difference was far more noticeable in Experiment 2. After five acquisition trials had occurred, the rate of button pressing during encoding actually attained the same level as that established at baseline. In other words, the participants rate of button pressing was hardly affected by the primary task of memorizing words once they had had more than one trial to see the words. However, the rate of button pressing during retrieval remained at the same level regardless of the number of acquisition trials for both groups. This rate began at a level that was approximately 60% of baseline and rose somewhat during the retrieval interval but always remained significantly below baseline for both groups regardless of the number of acquisition trials. Thus, our participants, amnesic patients and control subjects, seemed to try hard to exhaust their potential store of information regardless of the level they had attained during encoding. They did not just give up and pay more attention to the secondary task after they reached a point where they felt they had retrieved all they were going to be able to remember. What this means for theories of encoding and retrieval with amnesic patients is that we can now say with some confidence that the amnesic patient is not reducing the amount of relative effort expended on the primary task during either of these intervals of conscious information processing. We have stipulated elsewhere (Cermak, 1977; Cermak, Naus and Reale, 1976) that the quality of their effort during encoding is less than optimal when contrasted with the level attained by control subjects, but the quantity of effort is clearly present. Whatever the patient is doing while trying to memorize material at presentation, it requires as much attention as we see for normal individuals. We have also seen that this level of attention diminishes as the subject becomes more familiar with the material. Then, during retrieval, we have seen that the patient is making as much effort to retrieve, even though he is ultimately less successful, as do control subjects. The patient’s search process may not be as organized or controlled, but the patient does continue to attempt to recall material throughout the retrieval interval. Given this outcome, we can be reasonably certain that when future investigators of amnesic patients’ processing abilities try to measure the patients’ encoding and retrieval performance using single trial fMRI procedures (Buckner et al., 1996; D’Esposito et al., 1997; Schacter et al., 1997), the patients will at least be attempting to engage these processes. Then, if the same area of the brain activated during normal subject’s encoding (left prefrontal) is activated for amnesic patients during the same task, we can be reasonably certain that the patients are engaged in an on-line attempt to memorize that material. If the area is not activated in amnesia, then we can be certain that its nonactivation is not a consequence of lack of effort. We do not mean to imply that attention no longer needs to be assessed in future studies using fMRI procedures to study the way in which patients encode information. Instead, we strongly suggest that it would be reasonable to include divided attention tasks similar to the current one within any fMRI task so that the extent of effort directed toward the encoding task under investigation can be ascertained.
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Equally important, given that recent advances in fMRI and PET have established that the process of attempting to “retrieve” an item may be highly correlated with activation in the right prefrontal cortex (Tulving et al., 1994; Kapur et al., 1995; Schacter et al., 1996), we can now be certain that if amnesic patients demonstrate activation from that locus during retrieval that the activation is due to an attempt to retrieve as opposed to “correct” retrieval per se. This is because we have shown that the patients are expending effort during the retrieval interval even though they are highly unlikely to be correct in what they produce. The fact that amnesic patients try to perform during encoding and retrieval is important to demonstrate under the current experimental conditions and should be included during future on-line activation studies. Acknowledgments. This research was supported by the National Institute of Neurological Disorders and Stroke Program Project Grant NS 26985; by the National Institute of Alcohol and Alcohol Abuse grant AA 00187, both to Boston University School of Medicine, and by the Medical Research Service of the Department of Veterans Affairs. REFERENCES BUCKNER, R.L., BANDETTINI, P., O’CRAVEN, D., SAVOY, R., PETERSEN, S.E., RAICHLE, M.E., and ROSEN, B.R. Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. Proceedings of the National Academy of Science, 93: 14878-14883, 1996. CERMAK, L.S. The contribution of a “processing” deficit to alcoholic Korsakoff patients’ memory disorder. In I.M. Birnbaum and E.S. Parker (Eds.), Alcohol and Human Memory. Hillsdale, NJ: Lawrence Erlbaum, 1977. CERMAK, L.S., NAUS, M.J., AND REALE, L. Rehearsal and organizational strategies of alcoholic Korsakoff patients. Brain and Language, 3: 375-385, 1976. CRAIK, F.I.M., GOVONI, R., NAVEH-BENJAMIN, M., and ANDERSON, N.D. The effects of divided attention on encoding and retrieval processes in human memory. Journal of Experimental Psychology: General, 125: 159-180, 1996. D’ESPOSITO, M., ZARAHN, E., AGUIRRE, G.K., SHIN, R.K., AUERBACH, P., and DETRE, J.A. The effect of pacing of experimental stimuli on observed functional MRI activity. Neuroimage, 6: 113-121, 1997. FRIENDLY, M., FRANKLIN, P.E., HOFFMAN, D., and RUBIN, D.C. The Toronto Word Pool: Norms for imagery, concreteness, orthographic variables, and grammatical usage for 1,080 words. Behavior Research Methods and Instrumentation, 14: 375-399, 1982. KAPUR, S., CRAIK, F.I.M., JONES, C., BROWN, G.M., HOULE, S., and TULVING, E. Functional role of the prefrontal cortex in retrieval of memories: A PET study. Neuroreport, 6: 1880-1884, 1995. MEUDELL, P.R., MAYES, A.R., and MACDONALD, C. Dual task performance in amnesic and normal people: Does resource depletion cause amnesia? Cortex, 30: 159-166, 1994. SCHACTER, D.L., REIMAN, E., CURRAN, T., SHENG YUN, L., BANDY, D., MCDERMOTT, K.B., and ROEDIGER, H.L. Neuroanatomical correlates of veridical and illusory recognition memory: Evidence from Positron emission tomography. Neuron, 17: 1-20, 1996. SCHACTER, D.L., BUCKNER, R.L., KOUTSTAAL, W., DALE, A.M., and ROSEN, B. Late onset of anterior prefrontal activity during true and false recognition: An event-related fMRI study. Neuroimage, 6: 259-269, 1997. TULVING, E., KAPUR, S., CRAIK, F.I.M., MOSCOVITCH, M., and HOULE, S. Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission findings. Proceedings of the National Academy of Sciences, USA, 91: 2016-2020, 1994. WARRINGTON, E.K., and WEISKRANTZ, L. Further analysis of the prior learning effect in amnesic patients. Neuropsychologia, 16: 169-177, 1978. WECHSLER, D. Wechsler Adult Intelligence Scale-Revised. New York: The Psychological Corporation, 1981. WECHSLER, D. Wechsler Memory Scale-Revised. San Antonio, TX: The Psychological Corporation, 1987. Laird S. Cermak, Memory Disorders Research Center (151A), Department of Veterans Affairs Medical Center, 150 South Huntington Avenue, Boston, Massachusetts, 02130, U.S.A.; e-mail:[email protected]
(Received 24 March 1998; accepted 15 July 1998)
ABSTRACT This study examined the effect of divided attention during encoding or retrieval on primary (recall) or secondary (button-pressing) task performance by amnesic patients and control subjects. Experiment 1 demonstrated that control subjects’ recall was affected by divided attention during encoding but not during retrieval, while the amnesic patients’ recall remained at the same low level for all conditions. Both groups showed a reduction in rate of buttonpressing during encoding relative to their baseline levels and a further reduction during the retrieval interval. In Experiment 2, five learning trials, instead of just one, were presented. This acted to increase all subjects’ recall and also had the effect of producing superior recall following free encoding relative to encoding during divided attention for the amnesic patients as well as for the control subjects. Button-pressing performance during the encoding interval increased to baseline for both groups during the five presentation trials, but there was no increase in the rate of button-pressing during the retrieval interval. Amnesic patients’ normal attention to the primary task during encoding and retrieval was felt to have several implications for future neuroimaging tasks with these patients. Key words: amnesia, divided attention, encoding, retrieval
INTRODUCTION Chronic amnesic patients tend to become a bit passive in their interactions with members of their families or with the activities going on around them on a ward. Their affect often becomes more reactive than proactive and their response to general questions becomes limited to single word replies. Of course, this is understandable given their situation in which a link to the past and future has become extremely fragile and they seem to retain only the ability to live in the moment. Withdrawal into passivity and general observation of the passing scene is a reasonable response to years of confusion and frustration, even when those years are essentially forgotten altogether. It seems that the amnesic patient has given up trying to remember in many cases. This being the general case for many amnesic patients, one has to wonder to what extent this affect carries over to their tendency to try to perform well on a wide variety of memory tasks given to them over the months and years since they became amnesic. They appear to be motivated and willing to test, but to what extent are they really engaged in the activity and at least attempting to do the task at which they are failing so miserably? Every investigator of the amnesic syndrome knows that the patients is going to fail their recall or recognition task, but still must harbor thoughts of Cortex, (1999) 35, 73-87
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how hard the patient is actually trying in the face of such long term failure. This would be especially true for those patients who are quite aware of their disability. We have often had patients exclaim to us during testing that “This is exactly the kind of thing I can’t do”. Knowledge of the extent of involvement by the patient during a memory task would be most relevant when one is considering the relative contribution of amnesic patients’ depressed encoding and inadequate retrieval capabilities to the determination of their overall memory deficit (Cermak, 1977; Warrington and Weiskrantz, 1978). The question which has always been of some concern without ever being given much voice is whether or not the amnesic patient expends the same amount of effort that a normal subject commits to translating material into a form amenable to retrieval or in applying search strategies during retrieval. The difficulties an amnesic patient has encoding the properties of tobe-remembered information may emanate as much from a lack of effort committed to the translation as from an inability to perform such a tranformation. It is also possible that the amnesic patient may actually have suffered as much from an unwillingness to try to expend sufficient cognitive effort required to search their memory for the desired response during retrieval as for an inability to locate that information. These two possibilities have probably not been explored for two reasons: First, the patients appear to be highly diligent and attentive during both encoding and retrieval even when their daily affect has become rather lethargic, and second, there is no direct means of assessing this level of resource allocation. Recently, however, a paradigm which focuses on the amount of effort subjects expend on a secondary task during encoding and retrieval of to-beremembered material has been introduced by Craik et al. (1996). The paradigm utilizes a divided attention task in which the subject is asked to perform a secondary, ongoing task while also engaging in an attempt to encode or retrieve words. While the paradigm does not directly measure the amount of effort expended on the primary tasks of encoding and retrieval, it does require that the subject at least “divide” his attentional resources in order to try to optimize performance on the two tasks. If our amnesic patients expend little effort toward encoding the information, then their rate of secondary task performance will not be affected relative to baseline performance on the secondary task. Likewise, if the patients totally abandon the search process during the retrieval interval, then their rate of responding on the secondary task will not suffer. However, if the patients expend any amount of effort trying to perform the primary tasks of encoding or retrieving, then the rate of responding on the secondary task would decline during that interval. Determining whether or not the amount of effort the patients expend on the primary tasks is the same as normal control subjects would be important to know for two reasons: First, it is imperative that we determine that amnesic patients are putting forth normal effort during the processes of encoding and retrieval search before we ascribe too much credence to the lack of “quality” of their processing during these two stages of information processing. Second, investigators need to know that the patients are exerting as much effort into these processes as are normal control subjects when documenting the on-line
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processing abilities of amnesic patients using neuroimaging techniques such PET or fMRI. If the amnesic patient is not attempting to encode a word on any cognitive level, or is not trying to search for an item in memory using some strategy, even if deficient, then differences seen in their fMRI might not reflect real qualitative differences in the integrity of a mnemonic process so much as lack of effort on that level. Meudell, Mayes and MacDonald (1994) have shown that resource allocation may be a problem for amnesic patients on nonmnemonic tasks, so it becomes essential that we determine whether or not amnesic patients exert normal effort, as defined by allocation of resources, during the encoding and retrieval of verbal information. In order to investigate this ability, we adapted the Craik et al. (1996) divided attention paradigm for use with amnesic patients. EXPERIMENT 1 Materials and Methods Subjects The participants in this experiment consisted of two groups of amnesic patients and two control subject groups. Amnesic Korsakoff Patients. The first group of amnesic patients consisted of 8 men diagnosed with alcoholic Korsakoff syndrome, all residing at various private care facilities in the greater Boston area. All of these patients had a severe anterograde memory defect, as assessed by both clinical presentation and an extensive memory battery given at the Memory Disorders Research Center (MDRC). Prior to testing, these patients were presented at Memory Rounds and diagnosis unanimously confirmed by attending neurologists, neuropsychologists and staff members of the MDRC. All of the patients were unable to recall any day to day events, could not learn the names of individuals doing the testing, were somewhat disoriented in time and space and had extensive retrograde amnesia of varying lengths all being essentially complete for episodic material. The mean age for this patient group was 65 years, with a mean education level of 11.4 years. On the Wechsler Adult Intelligence Scale-Revised (Wechsler, 1981), the mean Verbal IQ for this groups was 92. On the Wechsler Memory Scale-Revised (Wechsler, 1987), the average Attention/Concentration index was 99, General Memory index was 79.1, and Delayed Memory index was 57.5. This patient group received a full battery of neuropsychological tests prior to experiment participation at the Memory Disorders Research Center. The patients scored significantly below normal on the Warrington Recognition of Faces and Words Test, the Rey Auditory Verbal Learning Test (RAVLT), the California Verbal Learning Test (CVLT) and Continuous Visual Memory Test (CVMT), and on retrograde memory assessments using the Boston Famous Faces and Events, Crovitz Autobiographical Questionnaire, and the Transient Events Test. On non-memory neuropsychological tests, subjects in this patient group scored at or above normal on the Boston Naming Test (BNT), Boston Diagnostic Aphasia Examination (BDAE), American National Adult Reading Test (ANART), Wide Range Achievement Test (WRAT), Line Orientation, Face Recognition, and Drawing tasks. Mixed Etiology Amnesic Patients. The second group of amnesic patients consisted of 4 men and 4 women with amnesias of varying etiologies. All eight patients who presented with amnesias were as dense clinically on the MDRC memory battery as the Korsakoff patients described above. Four of these patients became amnesic following anoxic episodes due to: an asthma attack in on case, a drug overdose in another case, and a massive myocardial infarction in the remaining two cases. Two patients
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became amnesic after contracting encephalitis with damage to the medial temporal lobes; one patient suffered a bilateral thalamic stroke; and one patient sustained a subarachnoid hemorrhage secondary to an aneurysm. The mean age for this group was 53.6 years, with a mean education level of 15.3 years. The mean WAIS-R Verbal IQ for this patient group was 102.3. The average Attention/Concentration index on the WMS-R was 99.4, the average General Memory index was 79.8, and the average Delayed Memory index was 60.1. This group also scored significantly below normal on the Warrington Recognition of Faces and Words test, the RAVLT, the CVLT, the CVMT and on our battery of retrograde memory tests. They scored normally on the BNT, the BDAE, the ANART, the WRAT, Line Orientation, Face Recognition and Drawing tasks. Alcoholic Control Subjects. The control group for the Korsakoff patients consisted of 8 chronic alcoholic controls (6 men, 2 women) living in private homes in the Boston area. None of these subjects showed any signs of neurological or psychiatric illness. All had abstained from alcohol consumption for at least six months prior to testing. Subjects in this group were matched with the Korsakoff amnesic group according to age, WAIS-R Verbal IQ, and education. The mean age of this group was 59.9 years, with a mean education level of 12.8 years. The average WAIS-R Verbal IQ for this group was 96.3. The average Attention/Concentration index on the WMS-R was 97.3, the average General Memory index was 103.3, and the average Delayed Memory index was 98.1. Normal Control Subjects. The control group for the mixed etiology amnesic patients consisted of 6 men and 2 women who had no prior history of alcohol abuse, neurological illness, or psychiatric disorder. Subjects in this group were matched with the mixed etiology amnesic group according to age, WAIS-R Verbal IQ, and education. The mean age of this group was 57.5 years, with a mean education level of 13.9 years. The average WAIS-R Verbal IQ for this group was 104.4. All normal control subjects were living in private homes in the Boston area. Stimuli The stimuli used in this experiment were two-syllable common concrete nouns selected from the Toronto Word Pool (Friendly et al., 1982). Stimuli were selected based on their average concreteness (on a scale of 1 to 7), with all of the words averaging 6.0 or higher. The stimuli were divided into 8 lists of 15 words each. An individual subject received only four word lists in this experiment, but all eight lists were used across subjects in this task and each word list was equally represented in each condition for all groups. Three of the four word lists that were not used in this experiment were later utilized in the second experiment that is reported in this manuscript. Design This was a Divided Attention experiment in which the subjects performed both a memory task and a button-pressing task. The memory task consisted of the experimenter reading a 15-word list to the subject, at a rate of 4 seconds per word. The subjects were then asked to recall as many of these words as possible during a 60-second retrieval interval. The subjects’ responses were recorded by the experimenter as the number correct given during each of six, 10-second intervals of the 60-second retrieval phase. The button-pressing task required that subjects view a display on the screen of a Macintosh Powerbook (using Psychlab software) and respond using a three-button button box. The visual display consisted of a row of three boxes shown across the screen with an asterisk programmed to appear randomly in one of the three boxes. The subject’s task was to press the button on the button box which corresponded to the position of the asterisk (i.e., if the asterisk appeared in the center box, the subject pressed the center button on the button box). A correct response by the subject resulted in the asterisk moving to a different box. An incorrect response had to be corrected before the asterisk would move to another box. Subjects were asked to perform as quickly and as accurately as possible, using their
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preferred hand. The asterisk was programmed never to appear in the same box on successive trials. Each subject performed in four different experimental conditions with a different word list used for each condition. The conditions consisted of combinations of divided attention (button-pressing) during either encoding or retrieval, during neither interval, or during both. Each subject participated in a condition of divided attention during the time that the material was being presented (divided attention at encoding) and a condition where the material was presented without distraction (free encoding). Likewise, the subject also participated in two retrieval conditions, one with divided attention (divided attention at retrieval) and one without distraction (free retrieval). The four conditions can be thought of as: 1) No divided attention at either encoding or retrieval, essentially a baseline condition. 2) Divided attention only at encoding and not at retrieval, which we refer to later as DA@Enc. 3) Divided attention only at retrieval and not at encoding i.e., DA@Ret. 4) Divided attention at both encoding and retrieval, i.e. DA@Enc. and DA@Ret. in the same condition. The order of the four experimental conditions was partially counterbalanced so that occurrence of each condition appeared equally often as the first, second, third or fourth task attempted. Procedure Each subject was tested individually in a private room accompanied by an Experimenter who administered instructions, initiated the preprogrammed experiment and recorded correct responses during the retrieval interval. Before beginning the actual experiment, each subject performed the button-pressing task for 60 seconds as practice and to familiarize them with the procedure. Then, subjects received their first experimental condition. Following the completion of this task, each subject was again asked to perform the button-pressing task for 60 seconds to obtain a baseline index of the subject’s button-pressing during the procedure free from having to perform the primary task. Next, each subject received the second experimental condition, after which there was a five-minute rest break. At the end of the break, each subject received the third experimental condition, followed by another 60-second button-pressing task, and finally, their fourth experimental condition. Thus, subjects performed the button-pressing task alone a total of three times during the entire experiment. The reaction times from the latter two of these instances was used as a baseline measure of each subject’s average button-pressing rate.
Results The Korsakoff patients and the mixed etiology amnesic patients were combined into one Amnesic group when preliminary analyses revealed no significant differences in performance between the two groups. This was true both for the number of words recalled by condition and for the number of button presses during each phase of the experiment. The alcoholic control subjects and the normal control subjects were also combined into one Control group because there were no significant differences in performance between these two groups for words recalled and for the number of button presses. During the recall phase, words produced by subjects that matched the target words were counted as correct responses. During all phases of the experiment, the number of button presses was recorded for each ten-second interval. Word Recall The mean number of correctly recalled words following the two conditions introduced at encoding (Divided Attention at Encoding and Free Encoding) and the two conditions at retrieval (Divided Attention at Encoding and Free
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Encoding) is shown for each group in Table I. An overall 2 × 2 × 2 ANOVA was performed on these scores using Group (Amnesic, Control) as the betweensubjects factor and the Encoding Conditions (Free, Divided) and Retrieval Conditions (Free, Divided) as within-subject factors. This analysis revealed a significant difference between Groups, F (1, 30) = 44.59, p < .01; between Encoding Conditions, F (1, 30) = 23.72, p < .01; and between Retrieval Conditions, F (1, 30) = 16.04, p < .01. In addition, one interaction achieved significance: Group × Encoding, F (1, 30) = 10.70, p < .01. The Triple interaction was not significant. TABLE I
Experiment 1 – Mean Number of Correctly Recalled Words as a Function of the Encoding (Free, Divided) or Retrieval (Free, Divided) Condition Encoding
Controls Amnesics
Retrieval
Free
DA
Free
DA
6.47 3.38
4.72 3.03
6.09 3.62
5.09 2.78
Simple effects revealed that the amnesic patients recalled fewer items than the control subjects both for the Free Encoding and for the Divided Attention at Encoding Conditions (both p’s < .01). The amnesic patients failed to show any differences between Encoding Conditions, while the control subjects recalled more items in the Free Encoding Condition (p < .01) than in the Divided Attention at Encoding Condition. This improvement by the control subjects probably accounted for most of the significant Group × Retrieval Condition Interaction. The Amnesic patients also recalled fewer items than the control subjects for both the Free Retrieval and Divided Attention at Retrieval Conditions (both p’s < .01). Both groups recalled more items during Free Retrieval than during Divided (p’s < .01) with no difference in the pattern of retrieval as evidenced by a lack of significance in the Group × Retrieval Condition Interactions. Button-Press Responding The mean number of button presses produced by each group during the two divided attention phases of the experiment (Encoding and Retrieval) as well as at Baseline is shown in Figure 1. A Group (Amnesic, Control) × Condition (Baseline, Encoding, Retrieval) ANOVA revealed a significant difference between Groups, F (1, 30) = 6.14, p < .05 and a significant difference between Conditions, F (2, 60) = 159.30, p < .01. The interaction between Group and Conditions was not significant. Simple effects revealed that the rate of button pressing differed between groups at both Baseline and Encoding (p’s < .05) but not during Retrieval. Rate of button pressing was significantly greater during the Baseline Interval than during Encoding for both Groups and for the Encoding interval relative to Retrieval interval for both Groups as well (p’s < .01).
Mean number of button presses
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Baseline (controls) DA@Enc. (controls) DA@Ret. (controls) Baseline (Amnesics) DA@Enc. (Amnesics) DA@Ret. (Amnesics)
Time interval Fig. 1 – The mean number of button presses per ten second interval for each group at baseline, simultaneous with encoding and with retrieval during Experiment 1.
A 2 × 3 × 6 ANOVA was also performed using Time Interval (10, 20, 30, 40, 50 and 60 secs.) as a within-subject factor in order to determine whether the rate of responding was constant within a condition. This analysis revealed a significant difference between Groups, F (1, 30) = 6.17, p < .05; Conditions, F (2, 60) = 159.28, p < .01; and Time Intervals, F (5, 150) = 30.78, p < .01. No interactions with Group attained significance, but the Condition × Time Interval interaction was significant, F (10, 300) = 11.71, p < .01. As can be seen in Figure 1, this interaction was primarily determined by the reduced responding that occurred during the first thirty seconds of Retrieval. The rate of responding across the other two conditions was relatively constant for both groups. Discussion The amnesic patients, as would be expected, recalled fewer words than did the control subjects across all the conditions of this experiment. More importantly though, the pattern of these amnesic patients’ recall differed somewhat from that of the control subjects. The control subjects recalled significantly more words when their attention was not divided during encoding than when it was divided, whereas the amnesic patients’ recall did not improve when encoding was performed without the restrictions imposed by having to simultaneously perform the secondary, button-pressing task. The amnesic patients’ recalled approximately the same number of items when they were free to attend solely to the words they had to remember and when they had to divide their attention betweeen this task and the button-pressing task. It was as if the additional time and/or resources available for the single task of encoding were not utilized as effectively for the amnesics as it was for the control subjects.
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The pattern of recall during free and divided attention conditions at retrieval was the same for both the amnesic patients and the control subjects. Both groups recalled more words when attention was not divided at retrieval than when it was. Craik et al. (1996) had reported that divided attention at retrieval did not have any effect for college students (only divided attention at encoding seemed to change these subjects’ recall ability). However, we found that divided attention at retrieval was nearly as detrimental as at encoding for our older and alcoholic subjects. The college students seemed able to overcome the interference produced from having to perform the secondary task during retrieval to a far greater extent than did our older subjects. Comparing the rate of performance on the button-pressing task for the two groups in our experiment, we found that the amnesic group performed below the control group throughout the experiment. They made significantly fewer button presses during the Baseline period and during the Encoding interval. At Retrieval the difference was again present, but this difference did not attain significance (p < .10). The pattern of responding across conditions was, however, precisely the same for both groups. The number of button presses during Encoding was less than during the Baseline, and the number of bar presses at Retrieval was smaller still. This latter effect was largely produced by the first half of the retrieval period (see Figure 1), as the subjects tried hardest to recall, but was still apparent throughout the retrieval interval. Even during intervals where subjects failed to retrieve a single word, their rate of button pressing remained below baseline. This outcome suggests that the amnesic patients were at least still trying to search for the words. Likewise, during the encoding interval, it has to be concluded that the amnesic patient is at least attending to the words since they do slow down somewhat on the secondary task. This does not mean that the amnesic patients’ encoding or retrieval strategies necessarily parallel those of the controls but rather that they are not ignoring the primary task. Given the rather low recall performance of all the subjects on this task, we feared that both the pattern of recall and the pattern of button pressing may have been a function of the low level of actual output of words for these subjects during retrieval. Since the subjects had so little information available to them with which to work, it seemed possible that the effect of recalling words on the secondary task had been underestimated. If the subjects had had more trials to learn the words then at the time of retrieval they may have had more information available to them to retrieve, and this, in turn might have resulted in greater impairment in the button-pressing performance. Alternatively, it could be that with better learning, the control subjects might find retrieval easier, as we have hypothesized was the case for college students in the Craik et al. (1996) experiment, and would then be free to devote more resource to the secondary task. This would be reflected in superior button-pressing performance for the control subjects relative to the amnesic patients, a result that did not occur with the low levels of item acquisition evident in Experiment 1. We also felt that if we provided more learning trials during the encoding condition, we might find less effect on the secondary task during the encoding interval as
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learning trials progressed. If less attention had to be paid to the encoding task, then more effort could be expended on the button pressing. To test these assumptions, we proceeded to give subjects five learning trials prior to their retrieval interval. EXPERIMENT 2 Materials and Method Subjects Amnesic Patient Group. The amnesic patient group consisted of seven men diagnosed with alcoholic Korsakoff syndrome and seven amnesic subjects with varying etiologies (4 men, 3 women). The mean age for the Korsakoff group was 67 years, with a mean education level of 11.3 years. On the Wechsler Adult Intelligence Scale-Revised (Wechsler, 1981), the mean Verbal IQ for this group was 91.7. On the Wechsler Memory Scale-Revised (Wechsler, 1987), the average Attention/Concentration index was 99.3, the average General Memory index was 78.4, and the average Delayed Memory index was 58.7. The mean age of the mixed etiology amnesic group was 53.6 years, with a mean education level of 15.7 years. The mean WAIS-R Verbal IQ for this patient group was 102. The average Attention/Concentration index on the WMS-R was 98.1, the average General Memory index was 78.6, and the average Delayed Memory index was 58.6. Control Subject Group. The control group for the amnesic patients consisted of 7 chronic alcoholic subjects (6 men, 2 women) and 7 normal control subjects (4 men, 3 women). The mean age of the alcoholic control group was 62.6 years, with a mean education level of 12.3 years. The mean WAIS-R Verbal IQ for this group was 98. The average Attention/Concentration index on the WMS-R was 103.4, the average General Memory index was 104.9, and the average Delayed Memory index was 100.4. The mean age for the normal control group was 55.3 years, with a mean education level of 14 years. The mean WAIS-R Verbal IQ for this group was 106.1. All normal control subjects were living in private homes in the Boston area. Stimuli The stimuli used in this experiment came from the same two-syllable common concrete nouns selected from the Toronto Word Pool (Friendly et al., 1982) used in Experiment 1. Specifically, each subject received three of the eight 15-word lists that he or she had not received in Experiment 1. This resulted in the same word lists being re-presented in both experiments without any individual ever encountering the same list. The lists were counterbalanced across all three conditions in this experiment just as they had been in Experiment 1. Design The design was identical to the one used in Experiment 1, with two exceptions. The first difference was that the word lists were read to subjects five times in a row during the free encoding and divided encoding phases, rather than just once. The second difference was that the divided attention at both encoding and at retrieval condition was not utilized in this study. Thus, each subject performed in three, rather than four, experimental conditions with one of the three different word lists used in each condition. Subjects received a Free Encoding-Free Recall task (Baseline condition), a Divided Attention at Encoding-Free Recall task (DA@Enc.), and a Free Encoding-Divided Attention at Recall (DA@Ret.) task. Before beginning the experiment, subjects performed the button-pressing task for 60 seconds as practice to familiarize the subject with the task. Then, the subjects received one of the three experimental conditions.
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Procedure Both the memory task and the button-pressing task were identical to those performed by subjects in Experiment 1. Since many of the amnesic patients participated in Experiment 1, at least two months intervened between test sessions. None of the control subjects had participated in Experiment 1.
Results Word Recall As in Experiment 1, the Korsakoff patients and the mixed etiology amnesic patients were combined into one Amnesic group when preliminary analyses revealed no significant differences in performance between the two groups. Similarly, the alcoholic control subjects and the normal control subjects were combined into one Control group since there were no significant differences in performance between these two groups. Encoding: The mean number of words correctly recalled following Free Encoding or Divided Attention (DA) at Encoding is shown for each group in Table II. An overall ANOVA performed on these scores using Group (Amnesic, Control) as the between-subjects factor and Encoding Condition (Free, DA at Encoding) as the within-subject factor revealed a significant difference between TABLE II
Experiment 2 – Mean Number of Correctly Recalled Words as a Function of the Divided Attention (DA) Condition: No DA, at Encoding (DA at Encoding) and at retrieval (DA at Retrieval)
Controls Amnesics
No DA
DA at Encoding
DA at Retrieval
9.64 4.93
7.57 3.57
9.57 5.00
Groups, F (1, 26) = 21.60, p < .01 and between Conditions, F (1, 26) = 14.64, p < .01. The Group × Encoding Condition interaction was not significant. Simple effects revealed that the amnesic patients recalled fewer items than the control subjects following each Encoding Condition (p’s < .01). Across conditions, both the amnesic patients and the control subjects recalled more items in the Free Encoding than in the DA at Encoding Condition (p’s < .05). Retrieval: The mean number of words correctly recalled during Free Recall or Divided Attention at Retrieval is also shown for each group in Table II. An overall ANOVA performed on these scores using Group (Amnesic, Control) as the between-subjects factor and Retrieval Condition (Free, DA at Retrieval) as the within-subject factor revealed a significant difference between Groups, F (1, 26) = 29.65, p < .01 but absolutely no difference (they were equal) between Conditions. The Group × Retrieval Condition interaction was also not significant. Simple effects revealed that the amnesic patients recalled fewer items than the control subjects for each Retrieval Condition (p’s < .01), but neither group demonstrated any difference in recall between the Free Recall and the DA at Retrieval Conditions.
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Divided Attention at Encoding Contrasted with Divided Attention at Retrieval: Recall following Divided Attention at Encoding relative to recall following Divided Attention at Retrieval could be compared in this paradigm by performing a Groups (Amnesic, Control) × Conditions (Free Encoding and Retrieval, DA et Encoding, DA at Retrieval) ANOVA. This analysis revealed a significant difference between Groups, F (1, 26) = 30.42, p < .01 and between Conditions, F (2, 52) = 9.48, p < .01. The interaction was not significant. Simple effects showed that the Group difference occurred at every Condition (p’s < .01). In addition, both Groups showed significantly less recall following DA at Encoding than during DA at Retrieval (p’s < at least .05). The recall following DA at Retrieval was actually as good as the Free Encoding-Free Retrieval Condition. Button-Press Responding
Mean number of button presses
The mean number of button presses produced by each group during the two divided attention phases of the experiment (Encoding and Retrieval) as well as at Baseline is shown in Figure 2. A Group (Amnesic, Control) × Condition (Baseline, Encoding, Retrieval) ANOVA revealed no significant difference between Groups (there had been a significant difference in Experiment 1), but a significant difference between Conditions, F (2, 52) = 135.32, p < .01 (as had been the case in Experiment 1). The interaction between Group and Conditions was significant, F (2, 52) = 3.58, p < .05 (this interaction had not been significant in Experiment 1). The difference in the number of button presses was never significantly different between Groups at any point. Thus, it appears that the significance was produced by the consistently faster responding by the control subjects relative to the amnesic patients during both the Baseline and the
Baseline (controls) DA@Enc. (controls) DA@Ret. (controls) Baseline (Amnesics) DA@Enc. (Amnesics) DA@Ret. (Amnesics)
Time interval Fig. 2 – The mean number of button presses per ten second interval for each group at baseline, simultaneous with encoding and with retrieval during Experiment 2.
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Encoding intervals but slower responding by the control subjects than by the amnesic patients during the Divided Attention at Retrieval interval. Overall the rate of responding was significantly greater during Baseline and Encoding for both Groups relative to the Retrieval interval (p’s < .01). A 2 × 3 × 6 ANOVA was also performed using Time Interval (10, 20, 30, 40, 50 and 60 secs.) as a within-subject factor in order to determine whether the rate of responding was constant within a condition. This analysis revealed no significant difference between Groups, F (1, 26) = 0.38. There was, however, a significant difference between Conditions, F (2, 52) = 122.52, p < .01; and Time Intervals, F (5, 130) = 32.82, p < .01. Both of the interactions with Condition attained significance: Group × Condition, F (2, 52) = 4.63, p < .01 and Condition × Time Interval, F (10, 260) = 11.82, p < .01. No other interactions were significant. As can be seen in Figure 2, the interactions were primarily determined by the slower rate of responding in the Retrieval Condition during the early intervals. Furthermore, this outcome was primarily determined by the Control Group as demonstrated by the significant Group × Condition interaction. The rate of responding across the other two conditions was relatively constant and this pattern was the same for both groups. Discussion As in Experiment 1, the amnesic patients recalled fewer words overall than did the control subjects. However, in the present experiment each group displayed the same pattern of recall performance. Recall of words was worse following divided attention during encoding than it was following the free encoding condition. However, recall was not significantly different for either group when divided attention occurred during the retrieval task than when retrieval was free. Contrasting recall between divided encoding and divided retrieval conditions revealed that divided attention at encoding disrupted recall to a significantly greater extent than divided attention at retrieval for both groups. In fact, as just noted above, divided attention at retrieval produced no noticeable effect on recall; only divided attention at encoding had this deleterious effect. The button pressing task also produced somewhat different results than had been reported for Experiment 1. In the present experiment, the amnesic patients’ performance was quite similar to that of the control subjects. There was no overall difference between the two groups in the number of button presses that were made across the entire experiment and no single point at which performance differed significantly. Both groups responded essentially the same during Encoding as they had during Baseline but significantly below this level during the Retrieval task. However, the two groups did not retain their same relative relationship across all three conditions resulting in the significant Group × Condition interaction. While the amnesic patients’ Baseline and Encoding button press rates were always below that of the control subjects, the amnesic patients’ rate of button pressing during Retrieval was above that of the control subjects. Thus, even though both groups slowed their rate of button pressing
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during the Retrieval stage, the control subjects must have done so to a significantly greater extent. This effect of slowing for retrieval extended across all time intervals but it was greatest during the first 30 seconds. GENERAL DISCUSSION The absolute number of words that amnesic patients were able to recall changed very little between Experiments 1 and 2 even though the paradigm used in the second experiment included five learning trials while the first had only one. However, the “pattern” of their recall did shift. In Experiment 1, there was no difference in recall between free encoding and encoding in the face of distraction from the secondary task. In Experiment 2, the amnesic patients demonstrated better retrieval under conditions of free encoding than they did under conditions of divided attention. This effect seemed to be largely produced by the fact that the patients were able to increase their retention from one learning trial to five when attention was not divided but could not do so under conditions of divided attention. The control subjects, on the other hand, demonstrated superior retrieval with no distraction relative to recall following divided attention at encoding after just one learning trial and retained the same relative difference between conditions following five learning trials even though the level of recall increased dramatically for both conditions. A more dramatic effect on recall performance following five learning trials occurred on the retrieval side for both groups. Following five learning trials, recall ability under the condition of divided attention was as good as recall when no secondary task was present. Following one learning trail (Experiment 1), divided attention at retrieval had produced a disruptive effect on the participant’s ability to recall the material. Thus, we found for both groups that divided attention at retrieval seems to have an effect on recall ability only for “underlearned” material, but has little effect on recall once that material has had the opportunity to be more fully acquired. Of utmost interest, is that this was true for the amnesic patients as well as for the control subjects. Obviously the amnesic patients did not acquire as much information as the control subjects, but apparently whatever level of acquisition they did attain stood up well in the face of distraction. This effect of level of acquisition on immunity to the distraction produced by divided attention did not occur for the college students in the original Craik et al. (1996) study. Those subjects demonstrated no effect of divided attention during retrieval on recall performance even though they had had only one acquisition trial. Apparently their subjects required only one presentation to acquire the material adequately. But clearly this was not the case for our older, and in some cases alcoholic, subjects or for our amnesic patients. It seems that our older subjects took more than one trial to achieve their maximum potential so that divided attention at retrieval would no longer have any effect on their recall. The results for the rate of button pressing during encoding or retrieval showed almost the mirror effect of that just described for recall when the
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increase from one learning trial to five is considered. For both the amnesic patients and the control subjects the rate of button pressing was slower during retrieval than during encoding, but the difference was far more noticeable in Experiment 2. After five acquisition trials had occurred, the rate of button pressing during encoding actually attained the same level as that established at baseline. In other words, the participants rate of button pressing was hardly affected by the primary task of memorizing words once they had had more than one trial to see the words. However, the rate of button pressing during retrieval remained at the same level regardless of the number of acquisition trials for both groups. This rate began at a level that was approximately 60% of baseline and rose somewhat during the retrieval interval but always remained significantly below baseline for both groups regardless of the number of acquisition trials. Thus, our participants, amnesic patients and control subjects, seemed to try hard to exhaust their potential store of information regardless of the level they had attained during encoding. They did not just give up and pay more attention to the secondary task after they reached a point where they felt they had retrieved all they were going to be able to remember. What this means for theories of encoding and retrieval with amnesic patients is that we can now say with some confidence that the amnesic patient is not reducing the amount of relative effort expended on the primary task during either of these intervals of conscious information processing. We have stipulated elsewhere (Cermak, 1977; Cermak, Naus and Reale, 1976) that the quality of their effort during encoding is less than optimal when contrasted with the level attained by control subjects, but the quantity of effort is clearly present. Whatever the patient is doing while trying to memorize material at presentation, it requires as much attention as we see for normal individuals. We have also seen that this level of attention diminishes as the subject becomes more familiar with the material. Then, during retrieval, we have seen that the patient is making as much effort to retrieve, even though he is ultimately less successful, as do control subjects. The patient’s search process may not be as organized or controlled, but the patient does continue to attempt to recall material throughout the retrieval interval. Given this outcome, we can be reasonably certain that when future investigators of amnesic patients’ processing abilities try to measure the patients’ encoding and retrieval performance using single trial fMRI procedures (Buckner et al., 1996; D’Esposito et al., 1997; Schacter et al., 1997), the patients will at least be attempting to engage these processes. Then, if the same area of the brain activated during normal subject’s encoding (left prefrontal) is activated for amnesic patients during the same task, we can be reasonably certain that the patients are engaged in an on-line attempt to memorize that material. If the area is not activated in amnesia, then we can be certain that its nonactivation is not a consequence of lack of effort. We do not mean to imply that attention no longer needs to be assessed in future studies using fMRI procedures to study the way in which patients encode information. Instead, we strongly suggest that it would be reasonable to include divided attention tasks similar to the current one within any fMRI task so that the extent of effort directed toward the encoding task under investigation can be ascertained.
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Equally important, given that recent advances in fMRI and PET have established that the process of attempting to “retrieve” an item may be highly correlated with activation in the right prefrontal cortex (Tulving et al., 1994; Kapur et al., 1995; Schacter et al., 1996), we can now be certain that if amnesic patients demonstrate activation from that locus during retrieval that the activation is due to an attempt to retrieve as opposed to “correct” retrieval per se. This is because we have shown that the patients are expending effort during the retrieval interval even though they are highly unlikely to be correct in what they produce. The fact that amnesic patients try to perform during encoding and retrieval is important to demonstrate under the current experimental conditions and should be included during future on-line activation studies. Acknowledgments. This research was supported by the National Institute of Neurological Disorders and Stroke Program Project Grant NS 26985; by the National Institute of Alcohol and Alcohol Abuse grant AA 00187, both to Boston University School of Medicine, and by the Medical Research Service of the Department of Veterans Affairs. REFERENCES BUCKNER, R.L., BANDETTINI, P., O’CRAVEN, D., SAVOY, R., PETERSEN, S.E., RAICHLE, M.E., and ROSEN, B.R. Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. Proceedings of the National Academy of Science, 93: 14878-14883, 1996. CERMAK, L.S. The contribution of a “processing” deficit to alcoholic Korsakoff patients’ memory disorder. In I.M. Birnbaum and E.S. Parker (Eds.), Alcohol and Human Memory. Hillsdale, NJ: Lawrence Erlbaum, 1977. CERMAK, L.S., NAUS, M.J., AND REALE, L. Rehearsal and organizational strategies of alcoholic Korsakoff patients. Brain and Language, 3: 375-385, 1976. CRAIK, F.I.M., GOVONI, R., NAVEH-BENJAMIN, M., and ANDERSON, N.D. The effects of divided attention on encoding and retrieval processes in human memory. Journal of Experimental Psychology: General, 125: 159-180, 1996. D’ESPOSITO, M., ZARAHN, E., AGUIRRE, G.K., SHIN, R.K., AUERBACH, P., and DETRE, J.A. The effect of pacing of experimental stimuli on observed functional MRI activity. Neuroimage, 6: 113-121, 1997. FRIENDLY, M., FRANKLIN, P.E., HOFFMAN, D., and RUBIN, D.C. The Toronto Word Pool: Norms for imagery, concreteness, orthographic variables, and grammatical usage for 1,080 words. Behavior Research Methods and Instrumentation, 14: 375-399, 1982. KAPUR, S., CRAIK, F.I.M., JONES, C., BROWN, G.M., HOULE, S., and TULVING, E. Functional role of the prefrontal cortex in retrieval of memories: A PET study. Neuroreport, 6: 1880-1884, 1995. MEUDELL, P.R., MAYES, A.R., and MACDONALD, C. Dual task performance in amnesic and normal people: Does resource depletion cause amnesia? Cortex, 30: 159-166, 1994. SCHACTER, D.L., REIMAN, E., CURRAN, T., SHENG YUN, L., BANDY, D., MCDERMOTT, K.B., and ROEDIGER, H.L. Neuroanatomical correlates of veridical and illusory recognition memory: Evidence from Positron emission tomography. Neuron, 17: 1-20, 1996. SCHACTER, D.L., BUCKNER, R.L., KOUTSTAAL, W., DALE, A.M., and ROSEN, B. Late onset of anterior prefrontal activity during true and false recognition: An event-related fMRI study. Neuroimage, 6: 259-269, 1997. TULVING, E., KAPUR, S., CRAIK, F.I.M., MOSCOVITCH, M., and HOULE, S. Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission findings. Proceedings of the National Academy of Sciences, USA, 91: 2016-2020, 1994. WARRINGTON, E.K., and WEISKRANTZ, L. Further analysis of the prior learning effect in amnesic patients. Neuropsychologia, 16: 169-177, 1978. WECHSLER, D. Wechsler Adult Intelligence Scale-Revised. New York: The Psychological Corporation, 1981. WECHSLER, D. Wechsler Memory Scale-Revised. San Antonio, TX: The Psychological Corporation, 1987. Laird S. Cermak, Memory Disorders Research Center (151A), Department of Veterans Affairs Medical Center, 150 South Huntington Avenue, Boston, Massachusetts, 02130, U.S.A.; e-mail:[email protected]
(Received 24 March 1998; accepted 15 July 1998)