Recall and Recognition Memory in Parkinson's Disease

RECALL AND RECOGNITION MEMORY IN PARKINSON'S DISEASE E. Kristin Breen O\ddenbrooke's Hospital, Cambridge)

INTRODUCTION

Contrary to Parkinson's original description of the disease of "the senses and intellects being uninjured" (Parkinson, 1817), more recent studies have reported substantial cognitive impairments in patients with Parkinson's disease. However, different studies have shown different degrees of impairments and the situation is still somewhat unclear both regarding the level of overall intellectual deterioration expected to occur in these patients (Dakof and Mendelsohn, 1986; Girotti, Soliveri, Carella et aI., 1988; Huber, Shuttleworth and Paulson, 1986; Pirozzolo, Hansch, Mortimer et aI., 1982), and the extent to which they are likely to show signs of frontal lobe type difficulties (Cools, van der Bercken, Horstink et aI., 1984; Gotham, Brown and Marsden, 1988; Lees and Smith, 1983; Miller, 1985; Taylor, Saint-Cyr and Lang, 1986). The latter have been attributed to a decrease in dopamine concentration in the prefrontal cortex in Parkinson's disease (Scatton, Rouqier, Javay-Agid et aI., 1982), and to subcortical deafferentation of the frontal lobes (Sagar, Sullivan, Gabrieli et aI., 1988). There has been little systematic work on difficulties associated with memory in Parkinson's disease. Memory is important in that it is involved in a number of different cognitive measures and features prominently in tests used to diagnose dementia. Most studies have used laboratory tasks. They have the advantage that they have been investigated in detail and the performance of normal subjects is well documented. A large number of studies within the experimental literature have been devoted to investigating the different processes involved in recall and recognition memory tests both at the time of learning and test. For example, Kintsch (1970) argued that recall involves two stages, a retrieval and a recognition or decision stage, while recognition involves only the latter. Other investigators have demonstrated that when subjects expect recall they engage in more active processing relying more on subvocal rehearsal and organisation of items than when they expect a recognition test (Hall, Grossman and Elwood, 1976; Lewis and Wilding, 1981). It has also been found that these strategies improve recall but not recognition performance (Bruce and Fagan, 1970; Estes and Dapolito, 1967; Kintsch, 1968). Recognition scores on the other hand, can be enhanced by increased item discriminability (Shepard, 1967). More recently, Hirst, JohnCortex, (1993) 29, 91-102

92

E.K. Breen

son, Kim et al. (1986), and Hirst, Johnson Phelps et al. (1988) reported that the recall of amnesic patients was disproportionately affected relative to recognition performance and concluded that amnesia selectively disrupts an aspect of memory critical to successful recall. Overall these results strongly suggest that different processes are involved in recall and recognition. Alternatively, similar processes may be involved but to a sufficiently different degree for the two paradigms to be affected differentially by the same experimental manipulations. On the basis of these studies it seems reasonable to assume that the attentional demands are likely to be greater for recall since this requires more active rehearsal and processing of the material to be remembered. Thus recall should be more affected by attentional impairments and particularly by impaired voluntary or internally driven attentional control. These processes may include the ability to adopt appropriate strategies and engage in more active manipulation of the material. In this respect they may be part of the Supervisory Attentional System described by Norman and Shallice (1980) which is sensitive to frontal involvement. Although as far as studies of frontal amnesia are concerned, it is not clear whether the difficulties observed in these patients are due to problems of organisation, storage and/or retrieval (Derouesne, Beauvois and Shallice, 1985; Milner, Petrides and Smith, 1985; Signoret and Lhermitte, 1976). In considering studies that are concerned with memory functions in Parkinson's disease, Flowers, Pearce and Pearce (1984) concluded that if there is a deficit it must begin at retrieval or a higher level processing stage. In addition, it was suggested by Weingartner, Burns, Diebel and Le Witt (1984) that patients with Parkinson's disease have difficulty with effort-demanding as opposed to automatic cognitive processing. Their results showed impairments on tasks where encoding was not facilitated by previously established relationships between items or by repeated presentation of the same items. These results are very similar to those reported for normal elderly subjects (Hultsch, 1974; Moenster, 1972; Smith, 1977). They suggest that patients with Parkinson's disease require more trials to reach a fixed learning criterion, and that although they can use associations between items when these are available, they appear to have difficulties producing their own associations when there are no obvious links between the items to be remembered. Alternatively, they may have difficulties in generating appropriate retrieval cues. The poor performance of the patient group reported by Weingartner et al. on serial recall, is certainly suggestive of difficulties in establishing inter-item relationships although it is not entirely clear from the results at what stage in the process this may have occurred. Serial position analysis of items in free recall is one method that has been used to look at qualitative differences in performance. Craik (1968) and Raymond (1971) reported that although elderly subjects showed as much recency as young subjects in free recall, they recalled fewer words from the beginning and middle portion of the list suggesting that they are limited in the amount of information they can establish in longer-term memory. Similar results were obtained by Spinnler, Della Sala, Bandera et al. (1988) comparing a group of patients suffering from senile dementia of the Alzheimer type to normal elderly controls. The poorer performance of the patients was ex-

Memory in Parkinson's disease

93

plained within the framework of Baddeley's (1983) model of working memory and in terms of impaired functioning of the central executive. Few analyses of this sort have been reported for patients with Parkinson's disease. One study reporting data on serial position effects was by Taylor, Saint-Cyr and Lang (1986). They found that both the primacy and recency effect were preserved in the Parkinson group but that they were impaired on words from the middle of the list. It was suggested that this reflected a frontal lobe type deficit. However, another possible explanation could be that this was due to a memory rather than frontal impairment and associated with limited capacity as a result of slowness in processing. As far as a frontal impairment is concerned one might have expected difficulties in adopting or shifting between different strategies leading to impaired recall in the very beginning or at the end of a list. The alternative view is that the primacy and recency effects are automatic and not under any form of strategic control which seems unlikely in view of studies reported on normal subjects (Bernbach, 1975; Lewis and Wilding, 1981; Wixted and McDowell, 1989). In studies of recognition memory a number of investigators have failed to find a deficit in Parkinson's disease (As so, Crown, Russel et aI., 1969; Flowers, Pearce and Pearce, 1984; Lees and Smith, 1983, and others). Tweedy, Langer and McDowell (1982), on the other hand, reported that their patients were worse than the control subjects in recognising words that were repeated and in detecting synonyms. However, the subjects in Tweedy's study were required to carry out both tasks within the same experimental procedure. Instead of representing a recognition deficit as such, these results may reflect sensitivity to interference or inability to switch between tasks, a difficulty which has been associated with frontal lobe type problems. Of relevance here is a recent study by Sagar, Sullivan, Gabrieli et ai. (1988) where it was reported that the recency discrimination of patients with Parkinson's disease was disproportionately impaired relative to content recognition and the results linked to subcortical deafferentation of the frontal lobes. Although it has generally been assumed that patients with Parkinson's disease will show impairments in recall and not recognition, there do not appear to be any reports of studies directly comparing performance on both types of tasks. Claims that performance on these two tests differ have been based on completely different studies. Given that most groups of Parkinson patients show a wide range of abilities it is essential that comparisons of recall and recognition are carried out on the same group of SUbjects. This is important because when different performance measures are compared across different groups of subjects it is difficult to be sure that the differences between groups are not simply a consequence of, differing ability. It is also possible that recognition is less sensitive to impairments than recall and thus less likely to show any effects. In view of this it is obviously important to avoid ceiling effects. Another consideration of relevance to Parkinson's disease is whether the impairments observed in memory could be caused by other factors such as for example, depression or anticholinergic medication, both of which have been associated with memory impairments (Koller, 1984; Miller, Berrios and

94

E.K. Breen

Politynska, 1987; Stromgren, 1977). Clearly these are possibilities that should also be taken into account. Questions for Investigation

The purpose of the present research was to compare recall and recognition performance in patients with Parkinson's disease to that of a control group. The recall~recognition distinction is of clinical importance in that subjects who consistently do poorly on tests of recognition memory, usually patients with dementia or who are suffering from organic amnesia, are likely to have more severe problems and to need a different approach to their memory difficulties. In addition to a comparison of the overall recall and recognition scores, an analysis of the serial position data in free recall should help to answer questions of whether there are qualitative or quantitative changes in performance. For example, a selective impairment in the beginning, middle or towards the end of a list could be due to difficulties with the processes necessary for establishing or maintaining traces in long-term or short-term memory respectively. Alternatively, they could be due to difficulties in adopting appropriate learning strategies or using more than one strategy. Poor recall overall on the other hand, with little or no changes in primacy or recency, would suggest no such qualitative differences in performance. An attempt was also made to assess whether the patient group would show greater sensitivity than the control subjects to interference from previous list items. If so, one would expect a greater drop in performance between the first and the last of the lists to be remembered. The results of Tweedy et al. (1982) of impaired recognition and synonym detection raise the possibility that these patients may be more sensitive to certain types of interference. Alternatively their impaired performance in detecting synonyms could mean that they are less likely to process information according to their semantic properties, and more likely to code on the basis of physical characteristics. If this is the case then the patient group should show less semantic confusion and be less affected by the inclusion of synonyms in a recognition test. MATERIALS AND METHOD

Subjects

Patients who regularly attended the Neurology Outpatient Clinic at Addenbrooke's Hospital, Cambridge, were selected on the basis of information in their medical notes. Only patients with Parkinson's disease who satisfied the selection criteria described below were selected and this was approximately 113 of the patients who attended the clinic over a period of 6 months. Seventeen patients were selected in order to obtain a sample of 15 as two were unable to take part. The Parkinson group included 9 males and 6 females. The average age was 64 years and 9 months and ranged from 54 to 73 years. The average age of onset of the disease was 56 years, and the mean duration of illness 8 years and 9 months, with a range from 4 to 17 years. The following selection criteria were used: Patients with a history of CV A, a1cohol-

Memory in Parkinson's disease

95

ism or other neurological conditions were not included in the study. None of the patients had undergone thalamotomy or other surgical procedures for the relief of Parkinson symptoms. Patients were also excluded on the basis of medication-linked complaints of confusion, memory loss and/or hallucinations. Medication was not adjusted for the study and was that which produced the optimal therapeutic effect. Only three patients were treated with anticholinergic drugs (Benzhexol). Patients with significant emotional disturbance antedating the onset of the disease or patients who themselves or whose relatives had complained of difficulties associated with dementia or depression were not included in the study. All the patients included in the sample were living in their own homes. The control subjects, 6 males and 9 females, were drawn from the spouses of patients attending the ourpatient clinic. The average age of subjects in the control group was 64 years 6 months ranging from 52 to 72 years. Again subjects with a history of neurological or psychiatric illness were not included in the sample. The two groups were matched approximately for educational and socio-economic level. Both covered the range from unskilled to professional status but with a majority of white and blue collar workers. Informed consent for testing was obtained from all subjects. Materials

Three lists of 20 unrelated words were generated with a mean frequency of 60 per million (Thorndike and Lorge, 1944). Word frequency and the number of syllables were distributed evenly across lists which consisted mainly of one and two syllable words. Another sixty words were chosen for the recognition test, 20 for each list, again with frequency and syllable length matched across lists. For each of the recognition lists 10 of the fillers were unrelated to the words in the recall list while 10 were synonyms. The synonyms were taken from Wilding and Mohindra (1981; 1983), and Whitten, Suter and Frank (1979). The synonym ratings ranged from 4.87 to 6.71 on a scale from 1 to 7. Positioning of the words in the recognition test was random except for two constraints. It was ensured that synonyms never immediately followed each other, and half of the new members of each synonym pair were shown before the old and vice versa. The order of presentation of items within a list was the same for all subjects in recall and recognition. Procedure

Subjects were either tested in the outpatient clinic or arrangements were made to see them at home. They were first asked to read aloud 10 items from the Schonell Reading Test to rule out difficulties with reading or acuity. All subjects were then shown the three lists in a counterbalanced order. List order was controlled for by counterbalancing the presentation of each list across subjects and groups in a Latin Square Design. The words were shown at a rate of one every 3 seconds. Before presentation of the lists the subjects were told that there were 20 words in each list and that they would be asked to recall as many of these as they could remember. This was followed by a yes/no recognition test for the items in that list. RESULTS

Recall Data The total number of words recalled by subjects in the two groups in each of the twenty serial positions combined over the three lists, are shown in Figure 1. The numbers of words recalled from four serial position blocks of five words were then calculated and a 2)(3 x4 analysis of variance per-

96

E.K. Breen

35 30

q \

c 25

w

\

q

...I

~ 20

u

~ 15

0 z

10 5 0 1

2

3

4

5

6

7 8

9 10 11 12 13 14 15 16 17 18 19 20

SERIAL POSITION

Fig. 1 - Total number of words recalled by subjects in the Parkinson (.-e) and the Control Group (0- - - 0 ) in each of the twenty serial positions.

formed on the results. The analysis yielded a significant main effect of Group (F=15.81; d.f.=I, 28; p<0 .0004) , Presentation (F=4.25; d.f.=2, 56; p<0.02), and Serial Position (F= 15.91 ; d.f. = 3. 84; p
97

Memory in Parkinson's disease TABLE I

Percent Recalled from Each List Presentation

2

3

Mean

32 18 14

26 20

31 21 10

Presentation Control group Parkinson group Difference

34

24

10

6

output. However, the proportion of words linked together in their original order of presentation was found to be significantly greater for subjects in the control relative to the patient group (Mann Whitney U = 162.5; dJ. = 15, 15; p<0.05). This effect was due mainly to increased recall of order by the former in the first and the last five serial positions (U = 174.5; d.f. = 15, 15; p
Correct recogmtIOns, misses and false alarms were calculated for each subject, and the percent of words recognised minus false alarms can be found in Table II. A 2 X 3 (Group X Presentation) analysis of variance performed on these results produced no significant effects (Group F = 0.14; d.f. = 1, 28; p<0.7, Presentation F = 1.79; d.f. = 2, 56; p<0.2, and Group vs. Presentation F = 0.14; d.f. = 2, 56; p<0.9). Similarly, no significant differences emerged between the Parkinson and control group in values of d' (2.06 and 2.11) and 13 (1.95 and 1.89 respectively), and their performance on synonyms was identical over the three presentations. Thus the significant results observed in this study are limited to the recall data. TABLE II

Percent of Words Recognised Minus False Alarms List presentation Control group Parkinson group

72 73

2

3

Overall %

71

69 67

70

69

71

98

E.K. Breen

DISCUSSION

The present results show that, compared to the control subjects, the Parkinson group was impaired on tests of free recall but not on tests of recognition memory. In recall, significant main effects are reported for serial position and list presentation, but none of the interactions was statistically significant and no significant differences emerged in the serial position data. If, as suggested in the introduction, it is assumed that the primacy and recency effect in free recall are not automatic but require that appropriate strategies be adopted, then by showing these effects the subjects in the patient group have demonstrated the ability to select and use these strategies. Thus although this study was not designed to investigate frontal impairments, it could be argued that at this level at least there appears to be no indication of a frontal deficit. Other studies employing serial position analyses have reported poorer recall in the beginning and from the middle portion of lists in elderly subjects and in patients with Alzheimer's disease (Craik, 1968; Spinnler et aI., 1988; Raymond, 1971). The primacy and recency measures adopted in the present study are relatively conservative and if we take this into account, then these results are not incompatible with those of Spinnler et aI. where only the first word in the list was included in the primacy effect. For example, the largest difference between the Parkinson and control subjects in Figure 1 is between the first list items. Further analyses of output order and of the type and number of errors produced in recall revealed no differences between the two sets of subjects. However, when the proportion of words recalled together in their original order of presentation was calculated, a significant effect was obtained with the control group recalling more items in order in the beginning and towards the end of the lists. It seems likely therefore, that the greater ability of the control subjects to remember items together in chunks helped to improve their overall recall relative to the patient group. These results are in line with earlier suggestions that order information enhances recall but is of little significance for recognition performance (Lewis and Wilding, 1981). They are also consistent with the results obtained by Weingartner et aI. (1984) on serial recall, indicating that Parkinson patients have some difficulty in establishing inter-item relationships. In addition, the absence of any differences between the two groups in errors and output order further suggests that the impaired recall of the patient group was due to difficulties occurring at the level of input rather than output. The finding of equally efficient recognition performance would indicate that there were no difficulties at this level in the memory process. One possible explanation for these results is that, although, on the basis of the serial position data, the subjects in the two groups appear to be using very similar strategies, subjects in the Parkinson group may have been using these less efficiently than the control subjects. This could have been due to a slowing down of rehearsal processes as reflected by the reduced recall of order information, and resulting from a slowing of mental processes generally

Memory in Parkinson's disease

99

thus limiting the capacity of the memory system. Alternatively, the impaired performance of the patient group in recall may have been due to attentional limitations. The latter seems less likely for two reasons. Firstly, these patients were able to adopt and engage in appropriate strategies to some extent and secondly, they showed a high level of performance on the recognition items which included sixty distractors, thirty of which were synonyms. However, the possibility cannot be ruled out entirely as attentional factors are obviously implicated in this type of memory process and difficult to separate from it. Overall, the recall scores in the present study were quite low in both groups suggesting that they found the tests demanding. A correlation between age and recall was not statistically significant. Similarly, a correlation computed between recall and duration of illness was also nonsignificant. However, this is perhaps not surprising when taking into account that progression of the disease is likely to vary from patient to patient, and severity to be related to the rate at which the disease progresses. Only one of three patients on anticholinergic medication showed impairments in recall compared to the Parkinson group as a whole suggesting that the effect of the drug can be variable. The dosage levels of the three patients were reported as similar. No significant differences were observed between the Parkinson and the control group on tests of recognition memory. Their recognition scores were at a similar level, and the results do not appear to be subject to a ceiling effect. However, this is not to say that these patients would not show impairments on a more demanding test of recognition memory. The present results indicated that the patients were limited with respect to the amount of information that they could actively process and that this was why recall was more affected than recognition. If the recognition test was made more difficult by including more items, then it seems likely that the processing load would increase to a level were the Parkinson group would begin to show a deficit relative to normals. An analysis of the recognition scores in terms of false alarms produced no significant differences betwee.n the two groups, both of which showed the same degree of semantic confusion. Perhaps one potential difficulty with this measure is that the synonym test may not have been a very strong test of semantic processing. For example, because of the small number of errors produced by both groups on these items, it is not clear whether to assume that their ability to process information to a semantic level is satisfactory or at ceiling. However, other studies involving different methods have also found that Parkinson patients can use semantic processing when this is required (Miller and Morris, personal communication; Scholz and Sastry, 1985; Weingartner, Bums et aI., 1984). To summarise, it was found that the Parkinson group was impaired relative to the control subjects on tests of free recall but not on tests of recognition memory. It seems unlikely that these results are due to depression or anticholinergic medication because of the strict criteria used in selecting subjects for the study. In fact, additional analyses of the results suggest that

100

E.K. Breen

the most likely explanation of the impaired recall of the Parkinson group is in terms of mental slowness inducing a limit on the number of items that can be actively processed. In view of the stringent selection criteria used, the present group is likely to represent a relatively able sample of the Parkinson population as a whole, but was already starting to show signs of impairment. Clinically, patients with poor performance on tests of recall often complain of difficulties associated with everyday memory. Consideration of some of these patients' results strongly suggests that they would be likely to experience some difficulties in this respect, yet few problems were reported by the patients themselves or their relatives. One possibility is that these problems are overshadowed by their more obvious physical and social difficulties. For example, reports by Hyman (1972), Paulson (1981) and Singer (1973, 1974a, 1974b) suggest that patients often feel embarrassed, apathetic, inadequate, bored and lonely. Furthermore, Singer reported that the most salient predictors of psychological status were physical factors. There has been relatively little work on the social and psychological problems experienced by these patients. This is an area that needs to be developed further. More clinically oriented studies should help to identify difficulties at an earlier stage and to learn more about the practical problems that occur, what they are, and how they relate to performance on cognitive tests.

ABSTRACT

This study is concerned with recall and recognition memory in patients with Parkinson's disease. The results show that the Parkinson group was significantly impaired on tests of free recall compared to a group of age matched controls. By contrast, when given tests of recognition memory for the same items their performance was practically identical. In recall, significant main effects are reported for serial position and list presentation but no qualitative differences were observed between the two groups on these measures, both of which showed a primacy and recency effect. However, the control subjects recalled significantly more words in their original order of presentation than the patient group, a difference which appears to have occurred at the level of input. It was concluded that although the patient group was able to adopt and use similar strategies to the control subjects, they were less efficient in using these, a difficulty which was attributed to limited capacity due to mental slowness. Acknowledgements. This work was supported by the East Anglian Regional Health Authority. I want to thank Dr. E. Miller for his help in setting up the study and for his comments on an earlier version of this paper, and Drs. I.M.S. Wilkinson and C.M.C. Allen for permission to test patients in their outpatient clinic at Addenbrooke's Hospital, Cambridge. I am also very grateful to Dr. Roz McCarthy for her comments and suggestions.

REFERENCES

Asso, D., CROWN, S., RUSSEL, l.A., and LOGUE, V. Psychological aspects of the stereo-taxic treatment of Parkinsonism. British Journal of Psychiatry, 115: 541-553, 1969.

Memory in Parkinson's disease

101

BADDELEY, A.D. Working Memory. Philosophical transactions of the Royal Society London, B, 302: 311-324, 1983. BERNBACH, H.A. Rate of presentation in free recall: A problem for two-stage memory theories. Journal of Experimental Psychology: Human Learning and Memory, 104: 18-22, 1975. BRUCE, D., and FAGAN, RL. More on the recognition and free recall of organized lists. Journal of Experimental Psychology, 85: 153-154, 1970. COOLS, A.R, V AN DEN BERCKEN, J.H.L., HORSTINK, M.W.I., V AN SPAENDONCK, K.P.M., and BERGER, H.J.C. Cognitive and motor shifting aptitude disorder in Parkinson's disease. Journal of Neurology, Neurosurgery and Psychiatry, 47: 443-453, 1984. CRAIK, F.I.M. Two components in free recall. Journal of Verbal Learning and Verbal Behaviour, 7: 996-1004, 1968. DAKOF, G.A., and MENDELSOHN, G.A. Parkinson's disease: The psychological aspects of a chronic illness. Psychological Bulletin, 99: 375-387, 1986. DEROUESNE, J., BEAUVOIS, M.F., and SHALLICE, T. Confabulation following anterior arterial surgery. Journal of Clinical and Experimental Neuropsychology, 7: 175, 1985. ESTES, W.K., and DAPOLITO, F. Independent variation of information storage and retrieval processes in paired-associate learning. Journal of Experimental Psychology, 75: 18-26, 1967. FLOWERS, K.A., PEARCE, I., and PEARCE, J.M.S. Recognition memory in Parkinson's disease. Journal of Neurology, Neurosurgery and Psychiatry, 47: 1174-1181, 1984. GIROTTI, F., SOLIVERI, P., CARELLA, F., PICCOLO, I., CAFFARRA, P., MUSICCO, M., and CARACENI, T. Dementia and cognitive impairment in Parkinson's disease. Journal of Neurology, Neurosurgery and Psychiatry, 51: 1498-1502, 1988. GOTHAM, A.M., BROWN, RG., and MARSDEN, C.D. "Frontal" cognitive function in patients with Parkinson's disease "on" and "off' Levodopa. Brain, 111: 299-321, 1988. HIETANEN, M., and TERAvAINEN, H. Cognitive performance in early Parkinson's disease. Acta Neurologica Scandinavica, 73: 151-159, 1986. HALL, J.W., GROSSMAN, L.R., and ELWOOD, K.D. Differences in encoding for free recall vs. recognition. Memory and Cognition, 4: 507-513, 1976. HIRST, W., JOHNSON, M.K., KIM, J.K., PHELPS, E.A., RISSE, G., and VOLPE, B.T. Recognition and recall in amnesics. Journal of Experimental Psychology: Learning, Memory and Cognition, 12: 445-451, 1986. HIRST, W., JOHNSON, M.K., PHELPS, E.A., and VOLPE, B.T. More on recognition and recall in amnesics. Journal of Experimental Psychology: Learning, Memory and Cognition, 14: 758-762, 1988. HUBER, SJ., SHUTTLEWORTH, E.C., and PAULSON, G.W. Dementia in Parkinson's disease. Archives of Neurology, 43: 987-990, 1986. HULTSCH, D.F. Learning to learn in adulthood. Journal of Gerontology, 29: 302-308, 1974. HYMAN, M.D. Sociopsychological obstacles to I-DOPA therapy that may limit effectiveness in parkinsonism. Journal of the American Geriatric Society, 20: 200-208, 1972. KrNTSCH, W. Recognition and free recall of organized lists. Journal of Experimental Psychology, 78: 481-487, 1968. KrNTSCH, W. In D.A. Norman (Ed.), Models of Free Recall and Recognition. New York: Academic Press, 1970. KOLLER W.C. Disturbance of recent memory function in Parkinson's patients on anticholinergic therapy. Cortex, 20: 307-311, 1984. LEES A.J., and SMITH, E. Cognitive deficits in the early stages of Parkinson's disease. Brain, 106: 257-270, 1983. LEWIS, K., and WILDING, J. Influences of test expectations on memory processing strategies. Current Psychological Research, 1: 61-74, 1981. MILLER, E. Possible frontal impairments in Parkinson's disease: A test using a measure of verbal fluency. British Journal of Clinical Psychology, 24: 211-212, 1985. MILLER E., BERRIOS, G.E., and POLITYNSKA, B. The adverse effect of Benzhexol on memory in Parkinson's disease. Acta Neurologica Scandinavica, 1987. MILNER .B., PETRIDES, M., and SMITH, M.L. Frontal lobes and the temporal organisation of memory. Human Neurobiology, 4: 137-142, 1985. MOENSTER, P.A. Learning and memory in relation to age. Journal of Gerontology, 27: 361-363, 1972. MORTIMER, J.A., PIROZZOLO, F.J., HANSCH, E.C., and WEBSTER, D.D. Relationship of motor symptoms to intellectual deficits in Parkinson's disease. Neurology, 32: 133-137, 1982. NORMAN, D.A., and SHALLICE, T. Attention to action: Willed and automatic control of behaviour. Centre for Human Information Processing: Tecnical Report No. 99, 1980. PARKINSON, J. An Essay on the Shaking Palsy. London: Whittingham and Rowland, 1817. PAULSON, G.W. The psychological aspects of parkinsonism. Ohio State Medical Journal, 77: 711717, 1981.

102

E.K. Breen

PICCIRILLI, M ., PICCININ, G.L., and AGOSTINI, L. Characteristic clinical aspects of Parkinson patients with intellectual impairment. European Neurology, 23: 44-50, 1984. PIROZZOLO, FJ., HANSCH, E.C., MORTIMER, J.A., WEBSTER, D.D ., and KUSKOWSKI, M.A. Dementia in Parkinson's disease: A neuropsychological analysis. Brain and Cognition, 1: 71-83, 1982. RA YMOND, B. Free recall among the aged. Psychological Reports, 29: 1179-1182, 1971. SAGAR, HJ., SULLIVAN, E.V., GABRIELI, J.D.E., CORKlN, S., and GROW DON, J.H. Temporal ordering and short-term memory deficits in Parkinson's disease. Brain, 111: 525-539, 1988. SCATTON, B., ROUQIER, L., JAVAY-AGID, F., and AGID, Y. Dopamine deficiency in the cerebral cortex in Parkinson's disease. Neurology, 32: 1039-1040, 1982. SCHOLZ, O.B., and SASTRY, M. Memory characteristics in Parkinson's di sease. International Journal of Neuroscience, 27: 229-234, 1985. SHEPARD, R.N. Recognition memory for words, sentences and pictures. Journal of Verbal Learning and Verbal Behaviour, 6: 156-163, 1967. SIGNORET, J.L. , and LHERMITTE, F. The amnesic syndrome and the encoding process. In M.R. Rosenzweig and E.L. Bennett (Eds.), Neural Mechanisms of Learning and Memory. Cambridge, Mass.: MIT Press, 1976. SINGER, E. Social costs of Parkinson's disease. Journal of Chronic Disease, 26: 243-254, 1973. SINGER, E. The effect of treatment with levodopa on parkinson patients' social functioning and outlook on life. Journal of Chronic Disease, 27: 581-594, 1974a. SINGER, E. Premature social aging: The social-psychological consequences of a chronic illness. Social Science and Medicine, 8: 143-151, 1974b. SMITH, A.D. Adult age differences in cued recall. Developmental Psychology, 13: 326-331, 1977. SPINNLER, H., DELLA SALA, S., BANDERA, R., and BADDELEY, A. Dementia, ageing, and the structure of human memory. Cognitive Neuropsychology, 5: 193-211, 1988. STROMGREN, L.S. The influence of depression in memory. Acta Psychiatrica Scandinavica, 56: 109128, 1977. TAYLOR, A.E., SAINT-CRY, J.A., and LANG, A.E. Frontal lobe dysfunction in Parkinson's disease. The cortical focus of neostriatal outflow. Brain, 109: 845-883, 1986. THORNDIKE, E.L., and LORGE, I. The Teacher 's Word Book of 30,000 Words. New York: Columbia University, Teachers College, Bureau of Publications, 1944. TwEEDY, J.R., LANGER, K.G., and McDOWELL, F.H. The effect of semantic relations on the memory deficit associated with Parkinson's disease. Journal of Clinical Neuropsychology, 4: 235247, 1982. WEINGARTNER, H., BURNS, S., DIEBEL, R., and LE WITT, P.A. Cognitive impairments in Parkinson's disease: distinguishing between effort-demanding and automatic cognitive processes. Psychiatry Research, 11: 223-235, 1984. WHITTEN, W.B., SUTER, W.N., and FRANK, M.L. Bidirectional synonym ratings of 464 noun pairs. Journal of Verbal Learning and Verbal Behaviour, 18: 109-127, 1979. WILDING, J., and MOHINDRA, N. Ratings of the degree of synonymity of 279 noun pairs. British Journal of Psychology, 72: 231-240, 1981. WILDING, J. , and MOHINDRA, N . Preferred synonyms for each noun of 279 synonym pairs. British Journal of Psychology, 74: 91-106, 1983. WIXTED, J.T., and McDOWELL, J.J. Contributions to the functional analysis of single-trial free recall. Journal of Experimental Psychology: Learning, Memory and Cognition, 15: 658-697, 1989. Dr. E.K. Breen, Cambridge Neurosciences Centre, Department of Neurology, Level 5. Addenbrooke's Hospital, Hills Road, Cambridge CB2 2QQ, U.K.