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Material-specific deficits in “remembering” in patients with unilateral temporal lobe epilepsy and excisions
Neuropsychologia 40 (2002) 1335–1342
Material-specific deficits in “remembering” in patients with unilateral temporal lobe epilepsy and excisions David A. Moscovitch a,∗ , Mary Pat McAndrews a,b b
a Department of Psychology, University of Toronto, Toronto, Canada Neuroscience Program, University Health Network, Toronto Western Hospital, Toronto, Canada
Received 18 April 2001; accepted 2 November 2001
Abstract A growing body of research suggests that “remembering” and “knowing” may be dissociable aspects of recognition memory. Cognitive theorists have argued that the former reflects conceptual processing and is based on distinctive memory traces whereas the latter is associated with perceptual analysis and reflects fluency of processing. Here, we investigate whether this framework can account for memory deficits observed following right or left temporal lobe damage, as suggested by Blaxton and Theodore [Brain and Cognition 35 (1997) 5]. Recognition memory for faces and words was examined in patients with unilateral temporal lobe epilepsy or excisions (TLE) and controls using the “remember–know” recognition paradigm. Participants studied items under conditions designed to enhance either conceptual processing or focus their attention on superficial aspects of the items. For controls, there was an increase in “remember” responses following conceptually-based encoding for both words and faces. This enhancement was eliminated in patients with left TLE for words and those with right TLE showed a diminished effect for faces. This pattern indicates an impairment in the ability to benefit from conceptual encoding that is specific to material preferentially processed by the damaged hemisphere. Furthermore, this effect was only observed for “remember” responses, which are based on the participants’ ability to recollect specific contextual aspects of the original study experience. These data can be interpreted in relation to current theories of hippocampal function, which emphasize the critical role played by the hippocampus in relational memory formation and retrieval. We offer this as a novel interpretation of the “remember–know” literature. © 2002 Elsevier Science Ltd. All rights reserved. Keywords: Recognition; Memory; Conceptual; Hippocampus
1. Introduction Almost a century and a half of research has revealed that the left and right hemispheres of the brain are specialized for different aspects of cognitive functioning. Although most researchers concur that the two cerebral hemispheres differ in their processing capabilities, debate is ongoing about how best to characterize these differences. The material specificity hypothesis embodies the view that the hemispheres differ in what they process best, with the left hemisphere specializing in the processing of verbal material, and the right hemisphere in processing the non-verbal, perceptual details or spatial attributes of material. An alternate viewpoint is that the best way to characterize the hemispheric differences is in terms of how information is processed. This “modes of ∗ Corresponding author. Present address: Department of Psychology, Boston University, 4th Floor, 648 Beacon Street, Boston, MA 02215, USA. Tel.: +1-617-353-9610; fax: +1-617-353-9609. E-mail address: [email protected] (D.A. Moscovitch).
processing” account holds that the left hemisphere processes stimuli in a piecemeal, analytic, and temporally-based manner, whilst the right hemisphere analyzes information in a more holistic and parallel fashion (for reviews, see [1,4,35]). Hemispheric differences observed in memory tasks have typically been consistent with the material specificity hypothesis. Unilateral damage to the left temporal lobe has been found to impair selectively the learning and retention of verbal material (e.g. words, stories), and right temporal lobe lesions result in memory deficits for non-verbal information (e.g. spatial location, figural detail), while leaving verbal memory intact [24,32,33]. Much of this evidence is based on studies of patients with temporal lobe epilepsy in whom memory impairments are observed in conjunction with damage or dysfunction in mesial temporal regions even prior to surgical excision [2,15,19]. A recent study by Blaxton and Theodore [3] suggests that the pattern of results typically observed on verbal and non-verbal memory tasks may reflect a more basic difference in processing mode between the two hemispheres. In
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particular, they suggest that the left hemisphere may be responsible for encoding material in a conceptually based or “distinctive” fashion whereas the right hemisphere is more responsible for perceptually-based analyses that modulate “fluency” of processing. These conclusions were based on use of the “remember–know” recognition paradigm in patients with unilateral temporal lobe epilepsy or excisions. The “remember–know” procedure was originally developed by Tulving [42] to gain insight into the states of awareness experienced during recollection. The paradigm has been more fully developed in recent years by Gardiner and coworkers. The “remember–know” procedure, like a standard recognition test, requires participants to identify items that they had previously studied. However, rather than simply responding “yes” to recognized test items, participants are asked to distinguish between two qualitatively different recollective experiences: “remembering” and “knowing”. They are instructed to answer “remember” when they can consciously recollect the original presentation of an item by bringing to mind a specific aspect of the earlier experience of seeing the item. Conversely, they are told to respond “know” when they can assert confidently that the item is familiar and appeared on the study list, but are unable to recollect any aspect of the experience associated with its original presentation. Extensive research using this paradigm has revealed that “remember” and “know” responses can be dissociated under particular experimental conditions, and that these dissociations cannot be attributed merely to differences in confidence or a unitary dimension of trace strength [13]. Encoding manipulations that have been found to influence “remember” responses while having little effect on “know” responses include read-generate [10,13], levels of processing [10,36], full versus divided attention [14], and word frequency [12]. In contrast, “know” responses are selectively increased by masked priming [36], matching the modality across the study and test [16], and suppressing focal attention [29]. Other manipulations have produced opposing effects on the two kinds of responses. Findings of this nature include more “remember” responses when studied items were words versus more “know” responses when studied items were non-words [12], and more “remember” responses for items rehearsed in an elaborate fashion compared with more “know” responses following maintenance rehearsal [11]. Several theoretical interpretations have been offered to account for these data. Tulving [42] originally proposed that “remembering” is a product of the episodic memory system, while “knowing” is a reflection of the semantic memory system. In contrast to the memory systems approach, some investigators have preferred to distinguish between conceptually- and data-driven memory processes [22,39]. Gardiner and Parkin combined these two approaches into a theoretical model, which maintains that “remembering” is based on an episodic memory system that depends on conceptual processing, while “knowing” is based on a semantic memory system that relies on perceptual processing [14].
A more recent framework maintains that “remembering” an item is a reflection of the distinctiveness of the encoded information, and thus a product of manipulations that serve to enhance such distinctiveness. “Knowing”, on the other hand, is a reflection of the fluency with which the item is processed at test, and thus, this type of response will be influenced by the degree to which encoding and test operations conspire to enhance processing fluency [38]. By this account, it is generally the case that conceptual processing at study enhances distinctiveness whereas focusing on perceptual characteristics influences fluency of processing, but this is not a necessary correspondence [37]. Blaxton and Theodore [3] adopted this distinctiveness/fluency framework in examining the differential contributions of left and right temporal lobes to “remembering” and “knowing”. In their study, participants viewed a set of line drawings that were difficult to name, a type of material the authors argued should encourage perceptual processing. At test, the control participants and patients with the left temporal (LT) lobe epilepsy generated significantly more “know” than “remember” responses, whilst the patients with right temporal (RT) lobe epilepsy produced significantly more “remember” than “know” responses. A second study used an encoding manipulation that emphasized either the perceptual detail of stimuli (line count condition) or a categorical interpretation of items (e.g. judge whether the design was more similar to a “knee” or “hockey sticks”). Controls were sensitive to this manipulation, producing more “know” than “remember” responses in the line count condition and more “remember” than “know” responses in the label condition. However, there was a striking difference in the response patterns for the two temporal lobe groups. For the LT group, “know” responses predominated irrespective of encoding condition, and for the RT group, “remember” responses were consistently offered. The authors’ interpretation of these results was that patients with unilateral left temporal lobe lesions are impaired in their ability to process stimuli distinctively, and therefore, answer “know” even when the encoding conditions are designed to enhance distinctive processing. In contrast, patients with unilateral right temporal lobe lesions are limited in their sensitivity to perceptual fluency, and therefore, consistently answer “remember”, despite exposure to encoding conditions designed to increase perceptual fluency. The primary goal of the present study was to explore further Blaxton and Theodore’s [3] novel suggestion that the differences in patterns of performance on the “remember–know” paradigm between LTE and RTE patients are due to information processing impairments per se. In particular, we questioned whether this “mode of processing” account would hold for both verbal and non-verbal material. Our study combined both word and face stimuli with encoding conditions that were designed either to enhance conceptual processing or to focus on more superficial analysis of study materials. For sake of clarity, we will refer to these encoding conditions as the “conceptual”
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and “perceptual” manipulations, respectively. Recognition memory was tested using the “remember–know” procedure. In accord with previous research on the “remember–know” paradigm, we expected neurologically normal controls to generate more “remember” judgments for word or face stimuli studied in conditions designed to enhance conceptual encoding, and more “know” judgments for words or faces studied in conditions designed to enhance encoding of the surface features of the items. If Blaxton and Theodore’s [3] “modes of processing” account of laterality is correct, LT patients should demonstrate global impairments in conceptual processing, as reflected in fewer “remember” responses for both words and faces, even for items studied in conditions designed to enhance elaborate or distinctive encoding. RT patients should demonstrate global impairments in perceptual processing, and produce more “remember” than “know” judgments across all encoding conditions. On the other hand, the material-specific view would predict that LT patients should demonstrate general impairments in verbal memory, with reduced output of both “remember” and “know” judgments for words relative to faces, regardless of whether the material was processed in a perceptual or conceptual manner. By comparison, RT patients should show general impairments in non-verbal memory, and produce fewer “remember” and “know” responses for faces relative to words, regardless of encoding conditions.
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prior to testing. All patients that had undergone surgery were either seizure-free post-operatively or had a 75% reduction in seizure frequency. Five patients in each group had not yet undergone surgery; classification of seizure focus for these individuals was based on electroencephalography, neuroradiology, and neuropsychological testing. For these individuals, continuous EEG monitoring over 5–8 days established a unilateral temporal lobe ictal onset and interictal epileptiform discharges. Furthermore, all were deemed to have radiological evidence of mesial temporal sclerosis except for one patient (RTE) who had an arteriovenous malformation in the right uncus. Finally, neuropsychological data did not reveal any significant abnormalities that would be suggestive of extra-temporal or bitemporal dysfunction. This careful selection process was used to render the preand post-operative samples in each group as homogeneous as possible with respect to the locus of damage. Demographic information for participants is presented in Table 1. Also displayed are relevant psychometric data for patients including full-scale IQ (WAIS-R or WAIS-III) and standardized scores (z scores) representing delayed recall from WMS measures of paragraph recall and visual reproduction. As different versions of the WMS (WMS-R and WMS-III) were used across patients, z scores were calculated based on normative reference data provided in test manuals. 2.2. Materials
2. Methods 2.1. Participants Three groups of participants were involved in the study. All participants gave informed consent prior to the experiment in accord with a protocol approved by the Toronto Hospital Research Ethics Board. They comprised 12 patients (4 male and 8 female) with left temporal lobe epilepsy or excisions (LT), 12 patients (4 male and 8 female), with right temporal epilepsy or excisions (RT) and 12 neurologically normal controls (4 male and 8 female) matched for age and years of education. All but one participant in each group was right handed. Seven individuals in each patient group had undergone unilateral temporal lobe excisions (4–6 cm removal from the lateral convexity and 1–2 cm removal from medial structures) between 4 and 8 months
The non-verbal stimuli consisted of color frontal photographs of 76 male and female faces. The 76 items were divided into four base sets of 19 faces; 2 were presented at study (1 in each encoding condition) and 2 served as lures on the recognition test. Assignment of sets to study and test conditions was counterbalanced across participants. The verbal stimuli consisted of 108 high familiarity (range 400–700), low imagebility (range 100–350) words, which were selected from the Medical Research Council Psycholinguistics database. The words were typed in scripted font (Monotype Corsiva) to enhance salience of perceptual characteristics. The 108 items were divided into four base sets of 27 words each. Two sets were presented at study and the remaining two served as lures at test, with the assignment of sets to study and test conditions counterbalanced across subjects.
Table 1 Demographic characteristics of participants tested in the experiment Controls, mean (S.D.) Age Education WAIS-R/III full scale IQ Delayed recall stories (z) Delayed recall figures (z)
31.42 (9.69) 13.83 (2.29)
LT group, mean (S.D.) 37.25 13.75 93.25 −0.53 0.55
(6.85) (2.6) (6.22) (0.59) (0.87)
RT group, mean (S.D.) 33.75 14.25 99.75 0.19 −0.73
(9.49) (2.18) (10.71) (1.10) (1.22)
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2.3. Procedure For both faces and words, participants studied one of the base sets under instructions designed to focus on perceptual characteristics and the other base set in a condition designed to enhance conceptual processing. The order of these conditions was counterbalanced across subjects. For faces, in the “perceptual” condition, participants were instructed to decide whether the person in the picture was male or female. For the “conceptual” condition, they were instructed to decide whether the person seemed to them to be a “sporty-type”, “intellectual”, “party-goer”, or “homebody”. This task was adapted from an earlier study [28]. The participants were told that there were no correct answers, but to sort the faces into the categories that they believed were most appropriate. For both conditions, participants were given two items to practice. For words, the “perceptual” condition involved reading the printed word aloud. In the “conceptual” condition, an antonym of the target item was provided together with the first letter of the target word (e.g. hot—c). Participants were instructed to read the first word silently and then generate the opposite of that word out loud, beginning with the first letter that appeared on the card. The experimenter provided the target for any item the participant failed to generate, which was then repeated aloud before continuing. Two practice trials were provided for both conditions. The study phase was incidental in the sense that participants were not informed of the forthcoming recognition test. Study of both kinds of material occurred before the recognition tests. There was a delay of approximately 15 min between encoding and recognition. In the recognition test, the experimenter explained that half of the stimuli on the test had been presented earlier and half were new. Participants were instructed to respond with one of three options for each item: “new” if they believed that the item had not been studied earlier, “remember” if they could consciously recall the event of studying the item during the study phase, and “know” if they could confidently assert that the item had been presented earlier, but could not consciously recall particulars of this earlier presentation. Conscious recollection was described as evoking a particular association, image, or some other personal experience from the original presentation of the item, or the ability to recall something specific about the appearance or position of the item. Following Gardiner and Parkin [14], the experimenter provided the participants with everyday examples to help clarify the difference between “remember” and “know”. The participants were told that if asked what movie they saw last, they would probably “remember” it, because aspects of that experience would come to mind, including the name of the movie, where it was playing, whether the theater was crowded, etc. Alternatively, a “know” response was explained in terms of recognizing someone in the street but not remembering whom the person was, or being unable to recollect anything at all about them.
Following these instructions, participants were required to describe the task and the difference between “remember” and “know” responses in their own words. Once it had been established that the participants understood the two types of responses correctly, the experimenter gave the participants a few items to practice, consisting of previous practice items and some new items randomly mixed together. As a final check on the participants’ understanding of the response types, the experimenter asked them to explain the judgments they made on the practice items.
3. Results There were no significant differences between groups in age (F (2, 33) = 1.34, P > 0.05) or education (F (2, 33) = 0.154, P > 0.05). Patients demonstrated mild memory deficits in comparison with population norms, with LT patients showing selective verbal recall impairment, whereas RT patients had difficulty with non-verbal recall (see Table 1). A 2 (hemisphere) × 2 (material) ANOVA revealed a significant hemisphere by material interaction (F (1, 22) = 20.42, P < 0.01), indicating material-specific impairment on WMS tests. Results of the experimental memory tasks are presented in Table 2. Although the sample sizes are insufficient to separate the patient groups by surgical status for statistical tests, we provide separate scores for the pre- and post-surgical cases for the reader. All inferential statistics, however, were conducted on the combined scores for LT and RT groups. To directly compare word and face stimuli for our experimental task, proportion correct scores (hits minus false alarms) were used in the analyses. Separate analyses of variance were performed on “remember” and on “know” responses, with group (control, LT, and RT) as the between-subjects factor and encoding condition (perceptual and conceptual) and material (faces and words) as within-subjects factors. 3.1. Remembering A main effect of encoding condition was found (F (1, 33) = 89.30, P < 0.01), indicating that participants answered “remember” more often for those items that were encoded conceptually compared with those items that were encoded perceptually. In addition, the analysis yielded significant two-way interactions between material and group (F (1, 33) = 6.05, P < 0.01) and between material and encoding condition (F (1, 33) = 4.57, P < 0.05). Of greater interest was a significant three-way interaction between material, encoding condition, and group (F (2, 33) = 9.178, P < 0.01). Separate ANOVA’s were performed for each participant group to elucidate further the nature of this interaction. For the control group, there were significant main effects of material (F (1, 11) = 6.72, P < 0.05) and encoding condition (F (1, 11) = 33.99, P < 0.01), reflecting a greater
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number of “remember” responses for words over faces, and an increase in “remembering” items which were encoded conceptually compared with those which were encoded perceptually. There was no significant interaction between these factors, indicating that the encoding manipulation had similar effects for both words and faces. Analysis of the LT group data also revealed significant main effects of material (F (1, 11) = 7.99, P < 0.05) and encoding condition (F (1, 11) = 34.928, P < 0.01) as well as a significant interaction between these factors (F (1, 11) = 12.371, P < 0.01). This interaction reveals that conceptual encoding enhanced “remember” responses for faces (t (11) = 6.72, P < 0.01), but not for words (t (11) = 1.278, P > 0.05). Finally, the ANOVA performed on the RT data revealed a significant main effect of encoding condition (F (1, 11) = 22.28, P < 0.01), as well as a two-way interaction between material and encoding condition (F (1, 11) = 5.85, P < 0.05). This interaction indicates that the increase in “remember” responses following conceptual encoding was greater for words (t (11) = 4.21, P < 0.01) than it was for faces (t (11) = 3.16, P < 0.05), although both contrasts revealed a significant effect of encoding condition. For false alarms, there was a main effect of group (F (2, 33) = 3.41, P < 0.05), with both patient groups producing more false alarms than controls. The material by group interaction was not significant (F (2, 33) = 1.28, P > 0.05) (see Table 2). 3.2. Knowing A repeated measures ANOVA revealed no significant main effects and no significant interactions between any of the variables. Thus, the proportion of correct “know” responses was not influenced by group, encoding condition, or material. There were also no main effects or interactions in the false alarm data (see Table 2).
Fig. 1. Remember rate (“remember”/(“remember”+“know”)) as a function of participant group.
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3.3. Remember rate To provide a more direct test of Blaxton and Theodore’s [3] conclusion that temporal lobe patient groups exhibit a global difference in remember and know judgments, we calculated the rate of “remember” responses (“remember”/“remember” + “know”) across encoding and material manipulations. These data are shown in Fig. 1. According to their account, we would expect this measure to be significantly elevated in RT patients and greatly reduced in LT patients in comparison with controls. A repeated measures ANOVA revealed no significant group effect (F (2, 33) = 0.51, P > 0.05), indicating no general trend for differential responding among the three groups.
4. Discussion Experiments utilizing the “remember–know” paradigm have demonstrated that when individuals encode information in a conceptual, elaborative manner, they are more likely to “remember” the event later [38]. The present study replicated this outcome in neurologically normal participants. However, the enhancement in remembering following conceptual processing was reduced or eliminated in patients with unilateral temporal lobe damage for material that was preferentially processed by the damaged region. That is, patients with left temporal lobe damage exhibited no improvement in their ability to “remember” words that they generated in comparison to those that they simply read, although they did benefit from conceptual encoding for faces. Similarly, for RT patients, the enhancement in “remember” responses under conceptual encoding was marginal for faces, whereas for words, it was substantial. Blaxton and Theodore [3] argued that left hemisphere damage results in global deficits in conceptual or distinctive processing, while right hemisphere damage leads to global impairments in perceptual processing or fluency. According to Blaxton and Theodore, these impairments become manifested in the “remember–know” procedure as a significant decrease in “remember” responses across encoding conditions for patients with left temporal lobe damage, and a marked decrease in “know” responses across encoding conditions for patients with right temporal lobe damage. We found, however, that the deficits in both groups of patients with temporal lobe damage were confined to those conditions designed to enhance conceptual encoding, and were manifested in a significant decrease in the number of “remember” responses only. In addition, these processing impairments did not occur globally but, rather, were material-specific. The rather striking discrepancy between our results and those reported by Blaxton and Theodore [3] may be attributable to differences in patient characteristics, materials, encoding conditions, or the understanding of, and compliance with “remember–know” instructions, although no critical difference is obvious. Our findings are more
consistent with the general pattern of reduced “remember” responses for individuals with cerebral dysfunction involving (if not limited to) the temporal lobes, including patients with Alzheimer’s disease, schizophrenia, and amnesia [5,21,26,40]. Furthermore, preliminary data from functional brain mapping studies (with only verbal stimuli) do not indicate a clear pattern of hemispheric specialization in temporal regions for the two types of recollective responses [6,9,18]. Thus, while there is undoubtedly some type of processing explanation that underlies the hemisphere by material interaction that is frequently observed with unilateral temporal lobe damage, it is not likely to be the distinctiveness versus fluency dimension suggested by Blaxton and Theodore. The current findings may be considered in light of recent theories regarding the hippocampus and its role in learning and memory. In a recent review, McDonald et al. [30] contend that the majority of these theories propose that the hippocampus plays a central role in forming and consolidating associations between novel, distinct stimuli during encoding, and that it is critical for restoring appropriate contextual cues during conscious recollection. Thus, damage to this region produces deficits in relational learning, specifically the type of encoding that emphasizes the integration of multiple stimulus elements [7,8]. In the present study, participants were instructed to say that they “remembered” an item if that item evoked a particular association, image, or some other personal experience from its original presentation, or if the participants could recall something specific about the appearance or position of the item in space. Thus, the criteria for hippocampal involvement in a task may be contained within these instructions, which emphasize relational or contextual elements at recognition. The “conceptual” study conditions employed in this study likely encouraged the participants to form associations between stimuli (e.g. between the word that was generated and its opposite) and integrate their characteristics relative to one another (e.g. “is this person an intellectual or a homebody?”). Thus, to the extent that these conceptual encoding conditions provided a firm basis for forming associations between stimuli, it is understandable that patients with hippocampal damage would be impaired in their ability to form, consolidate, and later “remember” these associations. This conjecture is consistent with other findings of impaired relational memory processing associated with temporal lobe epilepsy [17], and with the modest correlations (R = 0.41, P < 0.05) we observed between a clinical measure that emphasizes conceptual memory processing (recall of stories) and the experimental condition that taps this most directly (“remember” responses for words encoded conceptually). The general hypothesis that the hippocampus mediates “remembering” but not “knowing” is supported by recent fMRI studies, which suggest that the hippocampus plays a significant role in retrieving memories that are based on conscious recollection, but is not necessary for recognition based on familiarity alone [9,27]. This proposal is also
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consistent with the notion that recollection and familiarity may each be mediated by distinct regions of the medial temporal lobe [34]. Of course, patients in the present study cannot be said to have exclusive hippocampal damage, particularly the post-operative group who underwent excision of temporal neocortex as well as hippocampus. Nonetheless, as the presence of mesial temporal damage was an inclusion criterion, it can be argued that at least this region was affected in all patients. In addition, examination of the data according to operative status does not reveal any striking pattern of difference between pre- and post-surgical cases. We have failed to observe differences in other studies of memory processing using the same criteria for patient selection [43]. Similarly, other research has found no significant change in memory performance following temporal lobe excisions when there is clear evidence of damage to the hippocampus as in mesial temporal sclerosis [20,31,41]. Future examination of patients with surgical lesions restricted to the hippocampus would be helpful in clarifying the relative contributions of lateral and mesial temporal regions to both “remembering” and “knowing”. These findings are also relevant to recent studies examining the contribution of recollection and familiarity to recognition in amnesic patients. As already noted, “remember” judgments are typically affected to a much greater extent than “know” decisions in patients with memory disorders. However, two studies found that “know” decisions or familiarity ratings are also reduced in patients with bilateral temporal lobe damage [26,44]. As our patients showed no deficits in “know” responses, it is possible that disruption to processes underlying “know” decisions may require more complete or bilateral damage to medial temporal lobe structures. Although an orderly pattern of results was obtained for “remember” responses, “know” responses were not affected by any of the experimental manipulations in our study. However, it should be noted that this type of single dissociation— in which certain manipulations increase “remember” responses while having little effect on “know” responses—has been reported frequently in the literature [10,12,14,23,36]. It is possible that the “perceptual” manipulations used here did little to enhance perceptual analysis of items beyond what would have happened if the participants merely viewed the stimuli with no specific orienting instructions. Different manipulations may have increased the possibility of obtaining material-specific deficits in “know” responses in the patient groups. As well, the procedure used in the recognition test may influence what is measured by a “know” response. Knowlton [25] argues that asking participants to respond “remember”, “know”, or “new” may not be as valid as a procedure in which participants answer “remember” or “know” only after indicating whether they recognized the item. The former process may increase false alarms rates for “know” responses, and encourage participants to operationalize the “remember” and “know” responses as high and low confi-
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dence ratings. Our study, like Blaxton and Theodore’s [3], employed the one-step method. An issue of concern in almost any study of this nature involves the subjective experience of the participants. For example, it is virtually impossible to ensure that the participants encode words in a strictly “verbal” manner, or faces in a purely “non-verbal” way. In addition, we occasionally found that it was difficult for some participants to appreciate the difference between “remember” and “know” upon hearing the instructions. Thus, it was necessary to employ several built-in “checks” which allowed the experimenter to determine that the participants understood what was expected of them. We strongly advise future researchers in this area to use such “checks”, and stress the importance of utilizing the standardized experimental instructions, originally published by Gardiner and Parkin [14]. The results reported in the present study provide a specific framework in which to understand the memory deficits of patients with unilateral temporal lobe damage. Our findings suggest that temporal lobe patients are impaired in their ability to process information in an elaborate way. This processing deficit was reflected in the patients’ inability to produce a greater number of “remember” responses for items studied in conceptual encoding conditions, which have been shown reliably to facilitate this type of conscious “remembering” in neurologically normal participants. Our results also support the material-specificity hypothesis of laterality, in that these processing impairments were only observed in verbal stimuli for patients with left temporal lobe damage, and only in non-verbal material for patients with right temporal lobe damage. Finally, these data are compatible with current theories of hippocampal function, which emphasize its role in contextual encoding and retrieval. Future research should focus on exploring further the unique contribution of the hippocampus to “remembering”, as it is conceptualized in the “remember–know” paradigm.
Acknowledgements For their contribution and time, we thank the patients and control participants. We also thank Stephen Taylor for his support and advice, Mary Jaciw for assistance in testing participants, and two anonymous reviewers for helpful suggestions. This research was compiled in partial fulfillment of requirements for an undergraduate independent project at the University of Toronto. This work was supported by a grant from the Clinical Neuroscience Research Fund of the University Health Network.
References [1] Banich MT. Hemispheric specialization. In: Banich MT, editor. Neuropsychology: the neural basis of mental function, vol. 3. Boston: Houghton Mifflin Company, 1997. p. 91–123.
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[2] Baxendale SA, Thompson PJ, Van Paesschen W. A test of spatial memory and its clinical utility in the pre-surgical investigation of temporal lobe epilepsy patients. Neuropsychologia 1998;36:591–602. [3] Blaxton TA, Theodore WH. The role of the temporal lobes in recognizing visuospatial materials: remembering versus knowing. Brain and Cognition 1997;35:5–25. [4] Bryden MP. Laterality: functional asymmetry in the intact brain. New York: Academic Press, 1982. [5] Dalla Barba G. Recognition memory and recollective experience in Alzheimer’s disease. Memory 1997;5:657–72. [6] Duzel E, Yonelinas AP, Mangun GR, Heinze J-J, Tulving E. Event-related brain potential correlates of two states of conscious awareness in memory. Proceedings of the National Academy of Sciences 1997;94:5973–8. [7] Eichenbaum H. Is the rodent hippocampus just for place? Current Opinion in Neurobiology 1996;6:187–95. [8] Eichenbaum H, Otto P, Cohen NJ. The hippocampus—what does it do? Behavioural and Neural Biology 1992;57:2–36. [9] Eldridge LL, Knowlton BJ, Furmanski CS, Bookheimer SY, Engel SA. Remembering episodes: a selective role for the hippocampus during retrieval. Nature Neuroscience 2000;3:1149–52. [10] Gardiner JM. Functional aspects of recollective experience. Memory and Cognition 1988;16:309–13. [11] Gardiner JM, Gawlick B, Richardson-Klavehn A. Maintenance rehearsal affects knowing, not remembering; elaborative rehearsal affects remembering, not knowing. Psychonomic Bulletin and Review 1994;1:107–10. [12] Gardiner JM, Java RI. Recollective experience in word and nonword recognition. Memory and Cognition 1990;18:23–30. [13] Gardiner JM, Java RI. Recognising and remembering. In: Collins AF, Gathercole SE, Conway MA, Morris PE, editors. Theories of memory, vol. 6. Hillsdale (NJ): Lawrence Erlbaum Associates, 1993. p. 163–88. [14] Gardiner JM, Parkin AJ. Attention and recollective experience in recognition memory. Memory and Cognition 1990;18:579–83. [15] Gleissner U, Helmstaedter C, Elger CE. Right hippocampal contribution to visual memory: a pre-surgial and post-surgical study in patients with temporal lobe epilepsy. Journal of Neurology, Neurosurgery and Psychiatry 1998;65:665–9. [16] Gregg VH, Gardiner JM. Recognition memory and awareness: a large effect of study-test modalities on “know” responses following a highly perceptual task. European Journal of Cognitive Psychology 1994;6:131–47. [17] Helmstaedter C, Gleissner U, DiPerna M, Elger CE. Relational verbal memory processing in patients with temporal lobe epilepsy. Cortex 1997;33:667–78. [18] Henson RNA, Rugg MD, Shallice T, Josephs O, Dolan RJ. Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. Journal of Neuroscience 1999;19:3962–72. [19] Hermann BP, Wyler AR, Richey ET, Rea JM. Memory function and verbal learning ability in patients with complex partial seizures of temporal lobe origin. Epilepsia 1987;28:547–54. [20] Hermann BP, Wyler AR, Somes G, Duhan C, Berry AD, Clement L. Declarative memory following anterior temporal lobectomy in humans. Behavioral Neuroscience 1994;108:3–10. [21] Huron C, Danion J-M, Giacomoni F, Grange D, Robert P, Rizzo L. Impairment of recognition memory with, but not without, conscious recollection in schizophrenia. American Journal of Psychiatry 1995;152:1737–42. [22] Jacoby L. Remembering the data: analyzing interactive processes in reading. Journal of Verbal Learning and Verbal Behaviour 1983;22:485–508. [23] Java RI. States of awareness following word stem completion. European Journal of Cognitive Psychology 1994;6:77–92. [24] Jones-Gotman M, Zatorre RJ, Olivier A, Andermann F, Cendes F, Staunton H, et al. Learning and retention of words and designs
[25]
[26]
[27]
[28]
[29]
[30]
[31] [32]
[33]
[34]
[35]
[36] [37]
[38]
[39]
[40]
[41]
[42] [43]
[44]
following excision from medial or lateral temporal lobe structures. Neuropsychologia 1997;35:963–73. Knowlton BJ. The relationship between remembering and knowing: a cognitive neuroscience perspective. Acta Psychologica 1998;98:253–65. Knowlton BJ, Squire LR. Remembering and knowing: two different expressions of declarative memory. Journal of Experimental Psychology: Learning, Memory, and Cognition 1995;21: 699–710. Maguire EA, Faraneh V-K, Mortimer M. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 2001;124:1156–70. Mäntylä T. Recollections of faces: remembering differences and knowing similarities. Journal of Experimental Psychology: Learning, Memory, and Cognition 1997;23:1203–16. Mäntylä T, Raudsepp J. Recollective experience following suppression of focal attention. European Journal of Cognitive Psychology 1996;8:195–203. McDonald RM, Ergis A-M, Winocur G. Functional dissociation of brain regions in learning and memory: evidence for multiple systems. In: Foster JK, Jelicic M, editors. Memory: systems, process, or function? New York: Oxford University Press, 1999. p. 66–72. Miller LA, Munoz DG, Finmore M. Hippocampal sclerosis and human memory. Archives of Neurology 1993;50:391–4. Milner B. Hemispheric specialization: scope and limits. In: Schmitt FO, Worden FG, editors. The neurosciences: third study program, vol. 8. Massachusetts: MIT Press, 1974. p. 75–89. Morris RG, Abrahams S. Recognition memory for words and faces following unilateral temporal lobectomy. British Journal of Clinical Psychology 1995;34:571–6. Moscovitch M. Theories of memory and consciousness. In: Tulving E, Craik FIM, editors. Handbook of memory. Oxford: Oxford University Press, 1999. p. 609–25. Moscovitch M. Information processing and the cerebral hemispheres. In: Gazzaniga MS, editor. Handbook of behavioural neurobiology, vol. 2:13. New York: Plenum Press, 1979. p. 379–446. Rajaram S. Remembering and knowing: two means of access to the personal past. Memory and Cognition 1993;21:89–102. Rajaram S, Geraci L. Conceptual fluency selectively influences knowing. Journal of Experimental Psychology: Learning, Memory, and Cognition 2000;26:1070–4. Rajaram S, Roediger III HL. Remembering and knowing as states of consciousness during retrieval. In: Cohen JD, Schooler JW, editors. Scientific approaches to consciousness, vol. 11. Mahwah (NJ): Lawrence Erlbaum Associates, 1997. p. 213–40. Roediger III HL, Blaxton TA. Retrieval modes produce dissocations in memory for surface information. In: Gorfein DS, Hoffman RR, editors. Proceedings of the Ebbinghaus Centennial Conference on Memory and Cognitive Processes. Hillsdale (NJ): Lawrence Erlbaum Associates, 1987. p. 349–79. Schacter DL, Verfaillie M, Anes MD. Illusory memories in amnesic patients: conceptual and perceptual false recognition. Neuropsychology 1997;11:331–42. Seidenberg M, Hermann B, Wyler AR, Davies K, Dohan Jr FC, Leveroni C. Neuropsychological outcome following anterior temporal lobectomy in patients with and without the syndreom of mesial temporal lobe epilepsy. Neuropsychology 1998;12:303–16. Tulving E. Memory and consciousness. Canadian Psychology 1985;26:1–12. Viskontas IV, McAndrews MP, Moscovitch M. Remote memory deficits in patients with unilateral temporal lobe epilepsy and excisions. Journal of Neuroscience 2000;20:5853–7. Yonelinas AP, Kroll NEA, Dobbins I, Lazzara M, Knight RT. Recollection and familiarity deficits in amnesia: convergence of remember–know, process dissociation, and receiver operating characteristic data. Neuropsychology 1998;12:323–39.
Material-specific deficits in “remembering” in patients with unilateral temporal lobe epilepsy and excisions David A. Moscovitch a,∗ , Mary Pat McAndrews a,b b
a Department of Psychology, University of Toronto, Toronto, Canada Neuroscience Program, University Health Network, Toronto Western Hospital, Toronto, Canada
Received 18 April 2001; accepted 2 November 2001
Abstract A growing body of research suggests that “remembering” and “knowing” may be dissociable aspects of recognition memory. Cognitive theorists have argued that the former reflects conceptual processing and is based on distinctive memory traces whereas the latter is associated with perceptual analysis and reflects fluency of processing. Here, we investigate whether this framework can account for memory deficits observed following right or left temporal lobe damage, as suggested by Blaxton and Theodore [Brain and Cognition 35 (1997) 5]. Recognition memory for faces and words was examined in patients with unilateral temporal lobe epilepsy or excisions (TLE) and controls using the “remember–know” recognition paradigm. Participants studied items under conditions designed to enhance either conceptual processing or focus their attention on superficial aspects of the items. For controls, there was an increase in “remember” responses following conceptually-based encoding for both words and faces. This enhancement was eliminated in patients with left TLE for words and those with right TLE showed a diminished effect for faces. This pattern indicates an impairment in the ability to benefit from conceptual encoding that is specific to material preferentially processed by the damaged hemisphere. Furthermore, this effect was only observed for “remember” responses, which are based on the participants’ ability to recollect specific contextual aspects of the original study experience. These data can be interpreted in relation to current theories of hippocampal function, which emphasize the critical role played by the hippocampus in relational memory formation and retrieval. We offer this as a novel interpretation of the “remember–know” literature. © 2002 Elsevier Science Ltd. All rights reserved. Keywords: Recognition; Memory; Conceptual; Hippocampus
1. Introduction Almost a century and a half of research has revealed that the left and right hemispheres of the brain are specialized for different aspects of cognitive functioning. Although most researchers concur that the two cerebral hemispheres differ in their processing capabilities, debate is ongoing about how best to characterize these differences. The material specificity hypothesis embodies the view that the hemispheres differ in what they process best, with the left hemisphere specializing in the processing of verbal material, and the right hemisphere in processing the non-verbal, perceptual details or spatial attributes of material. An alternate viewpoint is that the best way to characterize the hemispheric differences is in terms of how information is processed. This “modes of ∗ Corresponding author. Present address: Department of Psychology, Boston University, 4th Floor, 648 Beacon Street, Boston, MA 02215, USA. Tel.: +1-617-353-9610; fax: +1-617-353-9609. E-mail address: [email protected] (D.A. Moscovitch).
processing” account holds that the left hemisphere processes stimuli in a piecemeal, analytic, and temporally-based manner, whilst the right hemisphere analyzes information in a more holistic and parallel fashion (for reviews, see [1,4,35]). Hemispheric differences observed in memory tasks have typically been consistent with the material specificity hypothesis. Unilateral damage to the left temporal lobe has been found to impair selectively the learning and retention of verbal material (e.g. words, stories), and right temporal lobe lesions result in memory deficits for non-verbal information (e.g. spatial location, figural detail), while leaving verbal memory intact [24,32,33]. Much of this evidence is based on studies of patients with temporal lobe epilepsy in whom memory impairments are observed in conjunction with damage or dysfunction in mesial temporal regions even prior to surgical excision [2,15,19]. A recent study by Blaxton and Theodore [3] suggests that the pattern of results typically observed on verbal and non-verbal memory tasks may reflect a more basic difference in processing mode between the two hemispheres. In
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particular, they suggest that the left hemisphere may be responsible for encoding material in a conceptually based or “distinctive” fashion whereas the right hemisphere is more responsible for perceptually-based analyses that modulate “fluency” of processing. These conclusions were based on use of the “remember–know” recognition paradigm in patients with unilateral temporal lobe epilepsy or excisions. The “remember–know” procedure was originally developed by Tulving [42] to gain insight into the states of awareness experienced during recollection. The paradigm has been more fully developed in recent years by Gardiner and coworkers. The “remember–know” procedure, like a standard recognition test, requires participants to identify items that they had previously studied. However, rather than simply responding “yes” to recognized test items, participants are asked to distinguish between two qualitatively different recollective experiences: “remembering” and “knowing”. They are instructed to answer “remember” when they can consciously recollect the original presentation of an item by bringing to mind a specific aspect of the earlier experience of seeing the item. Conversely, they are told to respond “know” when they can assert confidently that the item is familiar and appeared on the study list, but are unable to recollect any aspect of the experience associated with its original presentation. Extensive research using this paradigm has revealed that “remember” and “know” responses can be dissociated under particular experimental conditions, and that these dissociations cannot be attributed merely to differences in confidence or a unitary dimension of trace strength [13]. Encoding manipulations that have been found to influence “remember” responses while having little effect on “know” responses include read-generate [10,13], levels of processing [10,36], full versus divided attention [14], and word frequency [12]. In contrast, “know” responses are selectively increased by masked priming [36], matching the modality across the study and test [16], and suppressing focal attention [29]. Other manipulations have produced opposing effects on the two kinds of responses. Findings of this nature include more “remember” responses when studied items were words versus more “know” responses when studied items were non-words [12], and more “remember” responses for items rehearsed in an elaborate fashion compared with more “know” responses following maintenance rehearsal [11]. Several theoretical interpretations have been offered to account for these data. Tulving [42] originally proposed that “remembering” is a product of the episodic memory system, while “knowing” is a reflection of the semantic memory system. In contrast to the memory systems approach, some investigators have preferred to distinguish between conceptually- and data-driven memory processes [22,39]. Gardiner and Parkin combined these two approaches into a theoretical model, which maintains that “remembering” is based on an episodic memory system that depends on conceptual processing, while “knowing” is based on a semantic memory system that relies on perceptual processing [14].
A more recent framework maintains that “remembering” an item is a reflection of the distinctiveness of the encoded information, and thus a product of manipulations that serve to enhance such distinctiveness. “Knowing”, on the other hand, is a reflection of the fluency with which the item is processed at test, and thus, this type of response will be influenced by the degree to which encoding and test operations conspire to enhance processing fluency [38]. By this account, it is generally the case that conceptual processing at study enhances distinctiveness whereas focusing on perceptual characteristics influences fluency of processing, but this is not a necessary correspondence [37]. Blaxton and Theodore [3] adopted this distinctiveness/fluency framework in examining the differential contributions of left and right temporal lobes to “remembering” and “knowing”. In their study, participants viewed a set of line drawings that were difficult to name, a type of material the authors argued should encourage perceptual processing. At test, the control participants and patients with the left temporal (LT) lobe epilepsy generated significantly more “know” than “remember” responses, whilst the patients with right temporal (RT) lobe epilepsy produced significantly more “remember” than “know” responses. A second study used an encoding manipulation that emphasized either the perceptual detail of stimuli (line count condition) or a categorical interpretation of items (e.g. judge whether the design was more similar to a “knee” or “hockey sticks”). Controls were sensitive to this manipulation, producing more “know” than “remember” responses in the line count condition and more “remember” than “know” responses in the label condition. However, there was a striking difference in the response patterns for the two temporal lobe groups. For the LT group, “know” responses predominated irrespective of encoding condition, and for the RT group, “remember” responses were consistently offered. The authors’ interpretation of these results was that patients with unilateral left temporal lobe lesions are impaired in their ability to process stimuli distinctively, and therefore, answer “know” even when the encoding conditions are designed to enhance distinctive processing. In contrast, patients with unilateral right temporal lobe lesions are limited in their sensitivity to perceptual fluency, and therefore, consistently answer “remember”, despite exposure to encoding conditions designed to increase perceptual fluency. The primary goal of the present study was to explore further Blaxton and Theodore’s [3] novel suggestion that the differences in patterns of performance on the “remember–know” paradigm between LTE and RTE patients are due to information processing impairments per se. In particular, we questioned whether this “mode of processing” account would hold for both verbal and non-verbal material. Our study combined both word and face stimuli with encoding conditions that were designed either to enhance conceptual processing or to focus on more superficial analysis of study materials. For sake of clarity, we will refer to these encoding conditions as the “conceptual”
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and “perceptual” manipulations, respectively. Recognition memory was tested using the “remember–know” procedure. In accord with previous research on the “remember–know” paradigm, we expected neurologically normal controls to generate more “remember” judgments for word or face stimuli studied in conditions designed to enhance conceptual encoding, and more “know” judgments for words or faces studied in conditions designed to enhance encoding of the surface features of the items. If Blaxton and Theodore’s [3] “modes of processing” account of laterality is correct, LT patients should demonstrate global impairments in conceptual processing, as reflected in fewer “remember” responses for both words and faces, even for items studied in conditions designed to enhance elaborate or distinctive encoding. RT patients should demonstrate global impairments in perceptual processing, and produce more “remember” than “know” judgments across all encoding conditions. On the other hand, the material-specific view would predict that LT patients should demonstrate general impairments in verbal memory, with reduced output of both “remember” and “know” judgments for words relative to faces, regardless of whether the material was processed in a perceptual or conceptual manner. By comparison, RT patients should show general impairments in non-verbal memory, and produce fewer “remember” and “know” responses for faces relative to words, regardless of encoding conditions.
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prior to testing. All patients that had undergone surgery were either seizure-free post-operatively or had a 75% reduction in seizure frequency. Five patients in each group had not yet undergone surgery; classification of seizure focus for these individuals was based on electroencephalography, neuroradiology, and neuropsychological testing. For these individuals, continuous EEG monitoring over 5–8 days established a unilateral temporal lobe ictal onset and interictal epileptiform discharges. Furthermore, all were deemed to have radiological evidence of mesial temporal sclerosis except for one patient (RTE) who had an arteriovenous malformation in the right uncus. Finally, neuropsychological data did not reveal any significant abnormalities that would be suggestive of extra-temporal or bitemporal dysfunction. This careful selection process was used to render the preand post-operative samples in each group as homogeneous as possible with respect to the locus of damage. Demographic information for participants is presented in Table 1. Also displayed are relevant psychometric data for patients including full-scale IQ (WAIS-R or WAIS-III) and standardized scores (z scores) representing delayed recall from WMS measures of paragraph recall and visual reproduction. As different versions of the WMS (WMS-R and WMS-III) were used across patients, z scores were calculated based on normative reference data provided in test manuals. 2.2. Materials
2. Methods 2.1. Participants Three groups of participants were involved in the study. All participants gave informed consent prior to the experiment in accord with a protocol approved by the Toronto Hospital Research Ethics Board. They comprised 12 patients (4 male and 8 female) with left temporal lobe epilepsy or excisions (LT), 12 patients (4 male and 8 female), with right temporal epilepsy or excisions (RT) and 12 neurologically normal controls (4 male and 8 female) matched for age and years of education. All but one participant in each group was right handed. Seven individuals in each patient group had undergone unilateral temporal lobe excisions (4–6 cm removal from the lateral convexity and 1–2 cm removal from medial structures) between 4 and 8 months
The non-verbal stimuli consisted of color frontal photographs of 76 male and female faces. The 76 items were divided into four base sets of 19 faces; 2 were presented at study (1 in each encoding condition) and 2 served as lures on the recognition test. Assignment of sets to study and test conditions was counterbalanced across participants. The verbal stimuli consisted of 108 high familiarity (range 400–700), low imagebility (range 100–350) words, which were selected from the Medical Research Council Psycholinguistics database. The words were typed in scripted font (Monotype Corsiva) to enhance salience of perceptual characteristics. The 108 items were divided into four base sets of 27 words each. Two sets were presented at study and the remaining two served as lures at test, with the assignment of sets to study and test conditions counterbalanced across subjects.
Table 1 Demographic characteristics of participants tested in the experiment Controls, mean (S.D.) Age Education WAIS-R/III full scale IQ Delayed recall stories (z) Delayed recall figures (z)
31.42 (9.69) 13.83 (2.29)
LT group, mean (S.D.) 37.25 13.75 93.25 −0.53 0.55
(6.85) (2.6) (6.22) (0.59) (0.87)
RT group, mean (S.D.) 33.75 14.25 99.75 0.19 −0.73
(9.49) (2.18) (10.71) (1.10) (1.22)
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2.3. Procedure For both faces and words, participants studied one of the base sets under instructions designed to focus on perceptual characteristics and the other base set in a condition designed to enhance conceptual processing. The order of these conditions was counterbalanced across subjects. For faces, in the “perceptual” condition, participants were instructed to decide whether the person in the picture was male or female. For the “conceptual” condition, they were instructed to decide whether the person seemed to them to be a “sporty-type”, “intellectual”, “party-goer”, or “homebody”. This task was adapted from an earlier study [28]. The participants were told that there were no correct answers, but to sort the faces into the categories that they believed were most appropriate. For both conditions, participants were given two items to practice. For words, the “perceptual” condition involved reading the printed word aloud. In the “conceptual” condition, an antonym of the target item was provided together with the first letter of the target word (e.g. hot—c). Participants were instructed to read the first word silently and then generate the opposite of that word out loud, beginning with the first letter that appeared on the card. The experimenter provided the target for any item the participant failed to generate, which was then repeated aloud before continuing. Two practice trials were provided for both conditions. The study phase was incidental in the sense that participants were not informed of the forthcoming recognition test. Study of both kinds of material occurred before the recognition tests. There was a delay of approximately 15 min between encoding and recognition. In the recognition test, the experimenter explained that half of the stimuli on the test had been presented earlier and half were new. Participants were instructed to respond with one of three options for each item: “new” if they believed that the item had not been studied earlier, “remember” if they could consciously recall the event of studying the item during the study phase, and “know” if they could confidently assert that the item had been presented earlier, but could not consciously recall particulars of this earlier presentation. Conscious recollection was described as evoking a particular association, image, or some other personal experience from the original presentation of the item, or the ability to recall something specific about the appearance or position of the item. Following Gardiner and Parkin [14], the experimenter provided the participants with everyday examples to help clarify the difference between “remember” and “know”. The participants were told that if asked what movie they saw last, they would probably “remember” it, because aspects of that experience would come to mind, including the name of the movie, where it was playing, whether the theater was crowded, etc. Alternatively, a “know” response was explained in terms of recognizing someone in the street but not remembering whom the person was, or being unable to recollect anything at all about them.
Following these instructions, participants were required to describe the task and the difference between “remember” and “know” responses in their own words. Once it had been established that the participants understood the two types of responses correctly, the experimenter gave the participants a few items to practice, consisting of previous practice items and some new items randomly mixed together. As a final check on the participants’ understanding of the response types, the experimenter asked them to explain the judgments they made on the practice items.
3. Results There were no significant differences between groups in age (F (2, 33) = 1.34, P > 0.05) or education (F (2, 33) = 0.154, P > 0.05). Patients demonstrated mild memory deficits in comparison with population norms, with LT patients showing selective verbal recall impairment, whereas RT patients had difficulty with non-verbal recall (see Table 1). A 2 (hemisphere) × 2 (material) ANOVA revealed a significant hemisphere by material interaction (F (1, 22) = 20.42, P < 0.01), indicating material-specific impairment on WMS tests. Results of the experimental memory tasks are presented in Table 2. Although the sample sizes are insufficient to separate the patient groups by surgical status for statistical tests, we provide separate scores for the pre- and post-surgical cases for the reader. All inferential statistics, however, were conducted on the combined scores for LT and RT groups. To directly compare word and face stimuli for our experimental task, proportion correct scores (hits minus false alarms) were used in the analyses. Separate analyses of variance were performed on “remember” and on “know” responses, with group (control, LT, and RT) as the between-subjects factor and encoding condition (perceptual and conceptual) and material (faces and words) as within-subjects factors. 3.1. Remembering A main effect of encoding condition was found (F (1, 33) = 89.30, P < 0.01), indicating that participants answered “remember” more often for those items that were encoded conceptually compared with those items that were encoded perceptually. In addition, the analysis yielded significant two-way interactions between material and group (F (1, 33) = 6.05, P < 0.01) and between material and encoding condition (F (1, 33) = 4.57, P < 0.05). Of greater interest was a significant three-way interaction between material, encoding condition, and group (F (2, 33) = 9.178, P < 0.01). Separate ANOVA’s were performed for each participant group to elucidate further the nature of this interaction. For the control group, there were significant main effects of material (F (1, 11) = 6.72, P < 0.05) and encoding condition (F (1, 11) = 33.99, P < 0.01), reflecting a greater
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number of “remember” responses for words over faces, and an increase in “remembering” items which were encoded conceptually compared with those which were encoded perceptually. There was no significant interaction between these factors, indicating that the encoding manipulation had similar effects for both words and faces. Analysis of the LT group data also revealed significant main effects of material (F (1, 11) = 7.99, P < 0.05) and encoding condition (F (1, 11) = 34.928, P < 0.01) as well as a significant interaction between these factors (F (1, 11) = 12.371, P < 0.01). This interaction reveals that conceptual encoding enhanced “remember” responses for faces (t (11) = 6.72, P < 0.01), but not for words (t (11) = 1.278, P > 0.05). Finally, the ANOVA performed on the RT data revealed a significant main effect of encoding condition (F (1, 11) = 22.28, P < 0.01), as well as a two-way interaction between material and encoding condition (F (1, 11) = 5.85, P < 0.05). This interaction indicates that the increase in “remember” responses following conceptual encoding was greater for words (t (11) = 4.21, P < 0.01) than it was for faces (t (11) = 3.16, P < 0.05), although both contrasts revealed a significant effect of encoding condition. For false alarms, there was a main effect of group (F (2, 33) = 3.41, P < 0.05), with both patient groups producing more false alarms than controls. The material by group interaction was not significant (F (2, 33) = 1.28, P > 0.05) (see Table 2). 3.2. Knowing A repeated measures ANOVA revealed no significant main effects and no significant interactions between any of the variables. Thus, the proportion of correct “know” responses was not influenced by group, encoding condition, or material. There were also no main effects or interactions in the false alarm data (see Table 2).
Fig. 1. Remember rate (“remember”/(“remember”+“know”)) as a function of participant group.
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3.3. Remember rate To provide a more direct test of Blaxton and Theodore’s [3] conclusion that temporal lobe patient groups exhibit a global difference in remember and know judgments, we calculated the rate of “remember” responses (“remember”/“remember” + “know”) across encoding and material manipulations. These data are shown in Fig. 1. According to their account, we would expect this measure to be significantly elevated in RT patients and greatly reduced in LT patients in comparison with controls. A repeated measures ANOVA revealed no significant group effect (F (2, 33) = 0.51, P > 0.05), indicating no general trend for differential responding among the three groups.
4. Discussion Experiments utilizing the “remember–know” paradigm have demonstrated that when individuals encode information in a conceptual, elaborative manner, they are more likely to “remember” the event later [38]. The present study replicated this outcome in neurologically normal participants. However, the enhancement in remembering following conceptual processing was reduced or eliminated in patients with unilateral temporal lobe damage for material that was preferentially processed by the damaged region. That is, patients with left temporal lobe damage exhibited no improvement in their ability to “remember” words that they generated in comparison to those that they simply read, although they did benefit from conceptual encoding for faces. Similarly, for RT patients, the enhancement in “remember” responses under conceptual encoding was marginal for faces, whereas for words, it was substantial. Blaxton and Theodore [3] argued that left hemisphere damage results in global deficits in conceptual or distinctive processing, while right hemisphere damage leads to global impairments in perceptual processing or fluency. According to Blaxton and Theodore, these impairments become manifested in the “remember–know” procedure as a significant decrease in “remember” responses across encoding conditions for patients with left temporal lobe damage, and a marked decrease in “know” responses across encoding conditions for patients with right temporal lobe damage. We found, however, that the deficits in both groups of patients with temporal lobe damage were confined to those conditions designed to enhance conceptual encoding, and were manifested in a significant decrease in the number of “remember” responses only. In addition, these processing impairments did not occur globally but, rather, were material-specific. The rather striking discrepancy between our results and those reported by Blaxton and Theodore [3] may be attributable to differences in patient characteristics, materials, encoding conditions, or the understanding of, and compliance with “remember–know” instructions, although no critical difference is obvious. Our findings are more
consistent with the general pattern of reduced “remember” responses for individuals with cerebral dysfunction involving (if not limited to) the temporal lobes, including patients with Alzheimer’s disease, schizophrenia, and amnesia [5,21,26,40]. Furthermore, preliminary data from functional brain mapping studies (with only verbal stimuli) do not indicate a clear pattern of hemispheric specialization in temporal regions for the two types of recollective responses [6,9,18]. Thus, while there is undoubtedly some type of processing explanation that underlies the hemisphere by material interaction that is frequently observed with unilateral temporal lobe damage, it is not likely to be the distinctiveness versus fluency dimension suggested by Blaxton and Theodore. The current findings may be considered in light of recent theories regarding the hippocampus and its role in learning and memory. In a recent review, McDonald et al. [30] contend that the majority of these theories propose that the hippocampus plays a central role in forming and consolidating associations between novel, distinct stimuli during encoding, and that it is critical for restoring appropriate contextual cues during conscious recollection. Thus, damage to this region produces deficits in relational learning, specifically the type of encoding that emphasizes the integration of multiple stimulus elements [7,8]. In the present study, participants were instructed to say that they “remembered” an item if that item evoked a particular association, image, or some other personal experience from its original presentation, or if the participants could recall something specific about the appearance or position of the item in space. Thus, the criteria for hippocampal involvement in a task may be contained within these instructions, which emphasize relational or contextual elements at recognition. The “conceptual” study conditions employed in this study likely encouraged the participants to form associations between stimuli (e.g. between the word that was generated and its opposite) and integrate their characteristics relative to one another (e.g. “is this person an intellectual or a homebody?”). Thus, to the extent that these conceptual encoding conditions provided a firm basis for forming associations between stimuli, it is understandable that patients with hippocampal damage would be impaired in their ability to form, consolidate, and later “remember” these associations. This conjecture is consistent with other findings of impaired relational memory processing associated with temporal lobe epilepsy [17], and with the modest correlations (R = 0.41, P < 0.05) we observed between a clinical measure that emphasizes conceptual memory processing (recall of stories) and the experimental condition that taps this most directly (“remember” responses for words encoded conceptually). The general hypothesis that the hippocampus mediates “remembering” but not “knowing” is supported by recent fMRI studies, which suggest that the hippocampus plays a significant role in retrieving memories that are based on conscious recollection, but is not necessary for recognition based on familiarity alone [9,27]. This proposal is also
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consistent with the notion that recollection and familiarity may each be mediated by distinct regions of the medial temporal lobe [34]. Of course, patients in the present study cannot be said to have exclusive hippocampal damage, particularly the post-operative group who underwent excision of temporal neocortex as well as hippocampus. Nonetheless, as the presence of mesial temporal damage was an inclusion criterion, it can be argued that at least this region was affected in all patients. In addition, examination of the data according to operative status does not reveal any striking pattern of difference between pre- and post-surgical cases. We have failed to observe differences in other studies of memory processing using the same criteria for patient selection [43]. Similarly, other research has found no significant change in memory performance following temporal lobe excisions when there is clear evidence of damage to the hippocampus as in mesial temporal sclerosis [20,31,41]. Future examination of patients with surgical lesions restricted to the hippocampus would be helpful in clarifying the relative contributions of lateral and mesial temporal regions to both “remembering” and “knowing”. These findings are also relevant to recent studies examining the contribution of recollection and familiarity to recognition in amnesic patients. As already noted, “remember” judgments are typically affected to a much greater extent than “know” decisions in patients with memory disorders. However, two studies found that “know” decisions or familiarity ratings are also reduced in patients with bilateral temporal lobe damage [26,44]. As our patients showed no deficits in “know” responses, it is possible that disruption to processes underlying “know” decisions may require more complete or bilateral damage to medial temporal lobe structures. Although an orderly pattern of results was obtained for “remember” responses, “know” responses were not affected by any of the experimental manipulations in our study. However, it should be noted that this type of single dissociation— in which certain manipulations increase “remember” responses while having little effect on “know” responses—has been reported frequently in the literature [10,12,14,23,36]. It is possible that the “perceptual” manipulations used here did little to enhance perceptual analysis of items beyond what would have happened if the participants merely viewed the stimuli with no specific orienting instructions. Different manipulations may have increased the possibility of obtaining material-specific deficits in “know” responses in the patient groups. As well, the procedure used in the recognition test may influence what is measured by a “know” response. Knowlton [25] argues that asking participants to respond “remember”, “know”, or “new” may not be as valid as a procedure in which participants answer “remember” or “know” only after indicating whether they recognized the item. The former process may increase false alarms rates for “know” responses, and encourage participants to operationalize the “remember” and “know” responses as high and low confi-
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dence ratings. Our study, like Blaxton and Theodore’s [3], employed the one-step method. An issue of concern in almost any study of this nature involves the subjective experience of the participants. For example, it is virtually impossible to ensure that the participants encode words in a strictly “verbal” manner, or faces in a purely “non-verbal” way. In addition, we occasionally found that it was difficult for some participants to appreciate the difference between “remember” and “know” upon hearing the instructions. Thus, it was necessary to employ several built-in “checks” which allowed the experimenter to determine that the participants understood what was expected of them. We strongly advise future researchers in this area to use such “checks”, and stress the importance of utilizing the standardized experimental instructions, originally published by Gardiner and Parkin [14]. The results reported in the present study provide a specific framework in which to understand the memory deficits of patients with unilateral temporal lobe damage. Our findings suggest that temporal lobe patients are impaired in their ability to process information in an elaborate way. This processing deficit was reflected in the patients’ inability to produce a greater number of “remember” responses for items studied in conceptual encoding conditions, which have been shown reliably to facilitate this type of conscious “remembering” in neurologically normal participants. Our results also support the material-specificity hypothesis of laterality, in that these processing impairments were only observed in verbal stimuli for patients with left temporal lobe damage, and only in non-verbal material for patients with right temporal lobe damage. Finally, these data are compatible with current theories of hippocampal function, which emphasize its role in contextual encoding and retrieval. Future research should focus on exploring further the unique contribution of the hippocampus to “remembering”, as it is conceptualized in the “remember–know” paradigm.
Acknowledgements For their contribution and time, we thank the patients and control participants. We also thank Stephen Taylor for his support and advice, Mary Jaciw for assistance in testing participants, and two anonymous reviewers for helpful suggestions. This research was compiled in partial fulfillment of requirements for an undergraduate independent project at the University of Toronto. This work was supported by a grant from the Clinical Neuroscience Research Fund of the University Health Network.
References [1] Banich MT. Hemispheric specialization. In: Banich MT, editor. Neuropsychology: the neural basis of mental function, vol. 3. Boston: Houghton Mifflin Company, 1997. p. 91–123.
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[2] Baxendale SA, Thompson PJ, Van Paesschen W. A test of spatial memory and its clinical utility in the pre-surgical investigation of temporal lobe epilepsy patients. Neuropsychologia 1998;36:591–602. [3] Blaxton TA, Theodore WH. The role of the temporal lobes in recognizing visuospatial materials: remembering versus knowing. Brain and Cognition 1997;35:5–25. [4] Bryden MP. Laterality: functional asymmetry in the intact brain. New York: Academic Press, 1982. [5] Dalla Barba G. Recognition memory and recollective experience in Alzheimer’s disease. Memory 1997;5:657–72. [6] Duzel E, Yonelinas AP, Mangun GR, Heinze J-J, Tulving E. Event-related brain potential correlates of two states of conscious awareness in memory. Proceedings of the National Academy of Sciences 1997;94:5973–8. [7] Eichenbaum H. Is the rodent hippocampus just for place? Current Opinion in Neurobiology 1996;6:187–95. [8] Eichenbaum H, Otto P, Cohen NJ. The hippocampus—what does it do? Behavioural and Neural Biology 1992;57:2–36. [9] Eldridge LL, Knowlton BJ, Furmanski CS, Bookheimer SY, Engel SA. Remembering episodes: a selective role for the hippocampus during retrieval. Nature Neuroscience 2000;3:1149–52. [10] Gardiner JM. Functional aspects of recollective experience. Memory and Cognition 1988;16:309–13. [11] Gardiner JM, Gawlick B, Richardson-Klavehn A. Maintenance rehearsal affects knowing, not remembering; elaborative rehearsal affects remembering, not knowing. Psychonomic Bulletin and Review 1994;1:107–10. [12] Gardiner JM, Java RI. Recollective experience in word and nonword recognition. Memory and Cognition 1990;18:23–30. [13] Gardiner JM, Java RI. Recognising and remembering. In: Collins AF, Gathercole SE, Conway MA, Morris PE, editors. Theories of memory, vol. 6. Hillsdale (NJ): Lawrence Erlbaum Associates, 1993. p. 163–88. [14] Gardiner JM, Parkin AJ. Attention and recollective experience in recognition memory. Memory and Cognition 1990;18:579–83. [15] Gleissner U, Helmstaedter C, Elger CE. Right hippocampal contribution to visual memory: a pre-surgial and post-surgical study in patients with temporal lobe epilepsy. Journal of Neurology, Neurosurgery and Psychiatry 1998;65:665–9. [16] Gregg VH, Gardiner JM. Recognition memory and awareness: a large effect of study-test modalities on “know” responses following a highly perceptual task. European Journal of Cognitive Psychology 1994;6:131–47. [17] Helmstaedter C, Gleissner U, DiPerna M, Elger CE. Relational verbal memory processing in patients with temporal lobe epilepsy. Cortex 1997;33:667–78. [18] Henson RNA, Rugg MD, Shallice T, Josephs O, Dolan RJ. Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. Journal of Neuroscience 1999;19:3962–72. [19] Hermann BP, Wyler AR, Richey ET, Rea JM. Memory function and verbal learning ability in patients with complex partial seizures of temporal lobe origin. Epilepsia 1987;28:547–54. [20] Hermann BP, Wyler AR, Somes G, Duhan C, Berry AD, Clement L. Declarative memory following anterior temporal lobectomy in humans. Behavioral Neuroscience 1994;108:3–10. [21] Huron C, Danion J-M, Giacomoni F, Grange D, Robert P, Rizzo L. Impairment of recognition memory with, but not without, conscious recollection in schizophrenia. American Journal of Psychiatry 1995;152:1737–42. [22] Jacoby L. Remembering the data: analyzing interactive processes in reading. Journal of Verbal Learning and Verbal Behaviour 1983;22:485–508. [23] Java RI. States of awareness following word stem completion. European Journal of Cognitive Psychology 1994;6:77–92. [24] Jones-Gotman M, Zatorre RJ, Olivier A, Andermann F, Cendes F, Staunton H, et al. Learning and retention of words and designs
[25]
[26]
[27]
[28]
[29]
[30]
[31] [32]
[33]
[34]
[35]
[36] [37]
[38]
[39]
[40]
[41]
[42] [43]
[44]
following excision from medial or lateral temporal lobe structures. Neuropsychologia 1997;35:963–73. Knowlton BJ. The relationship between remembering and knowing: a cognitive neuroscience perspective. Acta Psychologica 1998;98:253–65. Knowlton BJ, Squire LR. Remembering and knowing: two different expressions of declarative memory. Journal of Experimental Psychology: Learning, Memory, and Cognition 1995;21: 699–710. Maguire EA, Faraneh V-K, Mortimer M. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 2001;124:1156–70. Mäntylä T. Recollections of faces: remembering differences and knowing similarities. Journal of Experimental Psychology: Learning, Memory, and Cognition 1997;23:1203–16. Mäntylä T, Raudsepp J. Recollective experience following suppression of focal attention. European Journal of Cognitive Psychology 1996;8:195–203. McDonald RM, Ergis A-M, Winocur G. Functional dissociation of brain regions in learning and memory: evidence for multiple systems. In: Foster JK, Jelicic M, editors. Memory: systems, process, or function? New York: Oxford University Press, 1999. p. 66–72. Miller LA, Munoz DG, Finmore M. Hippocampal sclerosis and human memory. Archives of Neurology 1993;50:391–4. Milner B. Hemispheric specialization: scope and limits. In: Schmitt FO, Worden FG, editors. The neurosciences: third study program, vol. 8. Massachusetts: MIT Press, 1974. p. 75–89. Morris RG, Abrahams S. Recognition memory for words and faces following unilateral temporal lobectomy. British Journal of Clinical Psychology 1995;34:571–6. Moscovitch M. Theories of memory and consciousness. In: Tulving E, Craik FIM, editors. Handbook of memory. Oxford: Oxford University Press, 1999. p. 609–25. Moscovitch M. Information processing and the cerebral hemispheres. In: Gazzaniga MS, editor. Handbook of behavioural neurobiology, vol. 2:13. New York: Plenum Press, 1979. p. 379–446. Rajaram S. Remembering and knowing: two means of access to the personal past. Memory and Cognition 1993;21:89–102. Rajaram S, Geraci L. Conceptual fluency selectively influences knowing. Journal of Experimental Psychology: Learning, Memory, and Cognition 2000;26:1070–4. Rajaram S, Roediger III HL. Remembering and knowing as states of consciousness during retrieval. In: Cohen JD, Schooler JW, editors. Scientific approaches to consciousness, vol. 11. Mahwah (NJ): Lawrence Erlbaum Associates, 1997. p. 213–40. Roediger III HL, Blaxton TA. Retrieval modes produce dissocations in memory for surface information. In: Gorfein DS, Hoffman RR, editors. Proceedings of the Ebbinghaus Centennial Conference on Memory and Cognitive Processes. Hillsdale (NJ): Lawrence Erlbaum Associates, 1987. p. 349–79. Schacter DL, Verfaillie M, Anes MD. Illusory memories in amnesic patients: conceptual and perceptual false recognition. Neuropsychology 1997;11:331–42. Seidenberg M, Hermann B, Wyler AR, Davies K, Dohan Jr FC, Leveroni C. Neuropsychological outcome following anterior temporal lobectomy in patients with and without the syndreom of mesial temporal lobe epilepsy. Neuropsychology 1998;12:303–16. Tulving E. Memory and consciousness. Canadian Psychology 1985;26:1–12. Viskontas IV, McAndrews MP, Moscovitch M. Remote memory deficits in patients with unilateral temporal lobe epilepsy and excisions. Journal of Neuroscience 2000;20:5853–7. Yonelinas AP, Kroll NEA, Dobbins I, Lazzara M, Knight RT. Recollection and familiarity deficits in amnesia: convergence of remember–know, process dissociation, and receiver operating characteristic data. Neuropsychology 1998;12:323–39.