Recall and recognition memory in patients with focal frontal, temporal lobe and diencephalic lesions

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Pergamon

PII] S9917Ð2821"87#99056ÐX

Neuropsycholo`ia\ Vol[ 25\ No[ 7\ pp[ 674Ð685\ 0887 Þ 0887 Elsevier Science Ltd[ All rights reserved Printed in Great Britain 9917Ð2821:87 ,08[99¦9[99

Recall and recognition memory in patients with focal frontal\ temporal lobe and diencephalic lesions MICHAEL D[ KOPELMAN and NICOLA STANHOPE Neuropsychiatry and Memory Disorders Clinic\ Division of Psychiatry and Psychology\ United Medical and Dental Schools of Guy|s and St Thomas|s Hospital\ St Thomas|s Campus\ London\ U[K[ "Received 06 July 0885^ accepted 10 October 0886#

Abstract*Patients with frontal\ temporal lobe\ or diencephalic lesions were compared with healthy controls on measures of recall and recognition memory for word lists[ Exposure times were titrated to match recognition memory scores 29 s after the end of word! list presentation as closely as possible[ Using this technique\ we failed to _nd a disproportionate impairment in recall memory in either the frontal lobe lesion patients or in the amnesic "temporal lobe and diencephalic# patients\ compared with healthy controls[ Consistent with this _nding\ performance on these tasks showed highly signi_cant correlations with anterograde memory quotients "despite the titration procedure#\ but not with executive:frontal function tasks[ On the other hand\ the frontal lobe lesion group showed disproportionate bene_t in the recall of semantically categorised words\ compared with unrelated words[ This may indicate an impairment in retrieval or access\ compared with the amnesic "temporal lobe and diencephalic# patients\ and:or an inability to organise their learning of unrelated words spontaneously\ compared with healthy controls[ Þ 0887 Elsevier Science Ltd[ All rights reserved[ Key Words] Amnesia^ executive^ semantic^ categorisation^ organisation^ learning[

patients with frontal lobe lesions have been confounded by {{ceiling e}ects|| during performance on recognition memory tests ð19Ł[ In fact\ it is quite di.cult to avoid either ceiling or ~oor e}ects in such studies[ Secondly\ Delbecq!Derouesne et al[ ð5Ł have described a patient with a frontal lobe lesion who showed a disproportionate impairment in recognition memory and\ consistent with this\ Kartsounis et al[ ð11Ł found that\ following frontal tractotomy\ patients showed statistically signi_cant de_! cits in recognition memory but not on measures of recall memory[ Thirdly\ in carefully controlled studies\ Hirst et al[ ð06\ 07Ł argued that amnesic patients in general show a disproportionate impairment in recall memory relative to recognition memory performance[ This _nding has been disputed by Haist et al[ ð05Ł but\ if correct\ it would suggest that disproportionate impairments in recall mem! ory are not con_ned to patients with frontal lobe lesions\ but may apply to amnesic patients in general[ These apparently con~icting _ndings would be rec! onciled if heterogeneity with respect to recall:recognition performance were clearly demonstrated in patients with frontal lobe lesions and:or other amnesic patients[ Con! sistent with the notion of heterogeneity\ we have recently found that it is only patients whose frontal lobe lesions invade the dorso!lateral cortical margins who show a

Introduction The contribution of the frontal lobes to memory\ and of frontal lesions to organic amnesia\ has been a matter of great interest of late in both neuropsychological and the neuro!imaging literature[ Neuropsychologists have attributed a wide range of highly speci_c memory and other cognitive processes to the frontal lobes ð13\ 30Ð 32Ł[ Positron emission tomography "PET# investigations during the performance of memory tasks by healthy sub! jects have revealed considerable frontal activation during both encoding and retrieval processes ð00\ 10\ 34Ł[ Consistent with many of these studies is the view that the frontal lobes play a particular role in recall memory\ which is more {{e}ortful|| and makes greater use of con! textual information and of conscious recollective pro! cesses than does recognition memory ð08\ 23\ 24\ 31Ł[ Against this\ some of the studies purporting to show disproportionate impairment in recall memory amongst

 To whom all correspondence should be addressed] Dr M[ D[ Kopelman\ United Medical and Dental Schools of Guy|s and St Thomas|s Hospital\ Division of Psychiatry + Psychology\ St Thomas|s Campus\ London SE0 6EH\ U[K[ Fax] 9060 522 9950^ E!mail] m[kopelmanÝumds[ac[uk

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M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

severe and disproportionate impairment in temporal con! text memory and that this does not occur in patients with more medially placed lesions ð29Ł[ Likewise\ the severity of impaired {{insight|| "or subjective evaluations of mem! ory# varies considerably amongst amnesic patients and is by no means uniform\ being correlated with a number of factors of which site of lesion is one ð17Ł[ Moreover\ some of the discrepancies within the existing literature on recall:recognition memory may result from the use of di}ering experimental procedures\ and from the prob! lems of ceiling and ~oor e}ects inherent in this type of study[ There is a lack of any studies speci_cally comparing recall and recognition in patients with focal frontal lesions and patients with lesions largely con_ned to either the diencephalon or the temporal lobes[ Consequently\ the purpose of the present study was to compare recall! :recognition memory performance in patients with focal frontal\ temporal lobe and diencephalic lesions\ using a protocol modi_ed from Hirst et al[ ð06\ 07Ł and designed to {{match|| recognition memory performance as closely as possible as well as to minimise ceiling:~oor e}ects[

Method Subject groups] clinical and CT scan description Patients were selected for having predominantly focal lesions producing memory impairment on clinical\ CT scan and "where relevant# EEG criteria[ As part of the research protocol\ they received an MRI "magnetic resonance# scan and a PET "posi! tron emission tomography# scan as well as cognitive assessment[ On the basis of our clinical and CT criteria\ we included for study 04 patients with diencephalic lesions\ 03 patients with temporal lobe lesions\ 04 with frontal lobe lesions and 19 heal! thy control subjects[ The 04 patients with diencephalic lesions included 02 patients who had an alcoholic Korsako} syndrome[ Twelve of these 02 patients had either a documented history or residual signs of a Wernicke episode which preceded their amnesic syndrome\ comparing favourably with other studies in which such features have been documented ð7\ 35Ł[ In all 02 patients\ memory was a}ected out of all proportion to any other cognitive de_cit ð15\ 35Ł[ In addition\ we included 1 patients who manifested an amnesic syndrome following surgical excision and irradiation of a Pituitary adenoma[ One of these patients has been described elsewhere ð03Ł] she had an IQ minus General MQ "memory quotient# discrepancy of 38 points\ whilst the other patient had an IQ minus General MQ discrepancy of 16 points[ Plotting the radiotherapy planning _elds against these patients| MRI scans indicated that structures a}ected by ×84) of the irradiation included the anterior thalamus\ the mammillary bodies\ the mammillo!thalamic tract and the fornix and it is plausible that these structures may also have been a}ected by ischaemia during the operation ð03Ł[ Hence\ these 1 patients were treated as cases of {{diencephalic|| amnesia[ The temporal lobe lesion patients included 8 patients with probable or de_nite "antibody con_rmed# herpes encephalitis\ all of whom had CT evidence of temporal lobe damage[ They also included 3 patients with hypoxic brain damage[ One of these patients became hypoxic following a heroin overdose and a period of prolonged unconsciousness] his CT scan showed enlargement of the temporal horns of the ventricles bilaterally\

indicating temporal lobe atrophy[ A second patient had attempted to hang himself and his initial CT scan showed a large area of infarction in the left temporal lobe[ A third patient showed left temporo!parietal infarction following a respiratory arrest[ The fourth patient developed amnesia after a prolonged period of unconsciousness of uncertain cause] although his CT scan showed nothing abnormal\ visual inspection of his PET was thought to show focal hypometabolism in the temporal lobes[ The _nal patient in the temporal lobe group had a pro! longed history of complex partial seizures with bilateral tem! poral lobe foci evident on EEG[ This patient|s CT scan showed some temporal lobe atrophy[ He was complaining of impaired memory\ but there was no evidence either at initial assessment or at "2!year# follow!up of generalised dementia[ The frontal lobe lesion group included 8 patients who were assessed 1 weeks following a bilateral frontal tractotomy[ In this operation\ yttrium rods are implanted in the frontal lobes for treatment of chronic a}ective disorders[ On MRI scan\ the yttrium rods could be seen in the medial and mid!frontal regions\ surrounded by a small area of radiation necrosis and a much larger area of oedema "see later#[ These patients were tested in the second post!operative week "or\ if there was pro! longed confusion\ in the third week#\ because in a longitudinal study\ Kartsounis et al[ ð11Ł found that these patients behaved most like patients with large frontal lesions at this time[ These patients had been on anti!depressant medication\ but the policy was to reduce the dose to a minimum shortly before surgery[ Despite this substantial dosage reduction\ Poynton et al[ ð27Ł demonstrated signi_cant improvement on the Hamilton Depression scale ð04Ł to fairly low "non!clinical# levels two weeks following surgery\ at which time Kartsounis et al[ ð11Ł found signi_cant impairments on executive:frontal lobe and recognition memory tests which had not been present before surgery[ Because these de_cits were not present either pre!oper! atively "despite severe depression# or 5 months later\ they have to be attributed to the new lesions\ rather than to the depression "which was much improved# or to the medication "which had been substantially reduced#[ In addition\ we examined 5 patients with focal frontal lesions[ One patient had old leucotomy scars from a bilateral operation in 0863 "i[e[ 07 years before testing# and the others had lesions resulting from a glioma\ haematoma\ infarcts\ or craniotomy[ Three of these 5 patients had right frontal lesions\ 0 had a left frontal lesion and 1 had bilateral lesions[ Three of these focal frontal patients had lesions extend! ing into the dorso!lateral frontal cortex^ the others had more medially sited lesions[

Subject groups] background neuropsychological _ndings Table 0 shows the mean age\ estimated premorbid IQ "NART!R# and current IQ "WAIS!R# across the patient groups ð26\ 37Ł[ The groups did not di}er signi_cantly in terms of either mean age\ NART!R IQ\ or current IQ\ although the frontal lobe group showed a mean NART!R minus IQ discrepancy of approximately 8[4 points\ against 7[9 points in the temporal lobe group\ 6[9 points in the diencephalic group and 1[1 points in the healthy controls[ Table 0 also shows mean immediate "general# and delayed memory quotients "GMQ and DMQ# in the subject groups on the WMS!R ð4Ł\ the overall ANOVAS and their statistical signi_cance[ The diencephalic and temporal lobe patient groups were severely and similarly impaired and this was con_rmed by Duncan|s Multiple Range post!hoc tests\ which demonstrated that both these groups di}ered signi_cantly from the controls "P ³ 9[94#\ but they did not di}er signi_cantly from each other in terms of either GMQ or DMQ[ The present sample of frontal lobe lesion patients showed a lesser but quite severe degree of memory impairment relative to healthy controls[ In terms of

M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

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Table 0[ Mean ages\ estimated premorbid IQ\ current full!scale IQ\ general memory quotients "GMQ# and delayed memory quotients "DMQ# across the 3 subject groups "20 SD# Healthy controls M Mean age Age range NART IQ "Premorbid# Current IQ "WAIS!R# General MQ "WMS!R# "GMQ# Delayed MQ "WMS!R# "DMQ#

S[D[

34[8 206[2 11Ð62 093[2 203[3 091[0 204[3 092[0 205[3 094[1 208[9

Frontal lobe patients M S[D[

Diencephalic patients M S[D[

Temporal lobe patients M S[D[

34[6 209[1 13Ð59 094[0 201[8 84[4 205[2 72[0 206[1 62[4 204[3

43[3 27[1 32Ð57 097[6 200[7 090[6 206[6 69[9 219[4 54[9 210[9

34[0 205[2 11Ð56 093[9 28[3 84[8 200[6 57[3 203[5 54[8 203[9

Duncan|s Multiple range post!hoc tests\ they di}ered sig! ni_cantly from controls "P ³ 9[94# for both GMQ and DMQ[ The frontal lobe group also di}ered signi_cantly from both the diencephalic and temporal lobe groups for GMQ but not DMQ[ The frontal lobe group|s mean IQ!GMQ di}erence was 01[3 points "203[4# against 20[6 points "28[5# in the diencephalic group and 16[4 points "208[4# in the temporal lobe group^ their IQ!DMQ di}erence was 10[8 points "200[7# against 25[6 "202[0# and 18[8 "207[1# respectively[ Perhaps more mean! ingfully\ their mean NART!GMQ di}erence was 11[0 points "202[5# against 27[6 "205[7# and 24[4 "210[4#^ and their mean NART!DMQ di}erence was 20[5 points "201[3# against 32[6 "207[7# and 27[64 "219[8#[ These _gures re~ect the fact that "i# we had selected for inclusion frontal lobe patients known to have memory complaints\ because we were interested in the nature of frontal memory impairment^ but also "ii# one would not expect a group of patients with frontal lesions to show so severe a memory impairment as patients with diencephalic or medial temporal lobe lesions[ Three tests of frontal lobe "{{executive||# function were admin! istered] FAS verbal ~uency ð3Ł\ card!sorting ð25Ł and cognitive estimates ð28Ł[ Low scores on the FAS test and on card!sorting categories are said to re~ect frontal impairment[ High scores on cognitive estimates and percentage perseverative scores on card!sorting "calculated according to Nelson|s ð25Ł procedure# re~ect frontal impairment[ The means\ standard deviations\ ANOVAS and signi_cance values on these tests are shown in Table 1[ The 3 groups di}ered signi_cantly across all the measures[ In terms of Duncan|s Multiple Range post!hoc tests\ the frontal group performed signi_cantly worse than the con! trols "P ³ 9[94# across all 3 measures and signi_cantly worse than the temporal lobe group at cognitive estimates[ The dien! cephalic group also performed signi_cantly worse than the con! trols in terms of percentage perseverations and cognitive estimates^ there were no other signi_cant di}erences[ However\

F

P

0[4

n[s[

9[6 9[8 04[1 19[5

n[s[ n[s[ ³9[990 ³9[990

when individual group comparisons were carried out by plan! ned t!tests\ the diencephalic group performed signi_cantly worse than the controls at cognitive estimates\ card!sorting categories and percentage perseverations\ and the temporal lobe group di}ered signi_cantly from controls at cognitive estimates "P ³ 9[94#[ The frontal lobe group again showed highly sig! ni_cant di}erences from controls on all 3 measures "P ³ 9[90 to P ³ 9[9990#\ but the frontal group also di}ered signi_cantly from the temporal lobe group on cognitive estimates "P ³ 9[94#[ Taken together\ these _ndings indicate that\ although patients with diencephalic or temporal lobe lesions can show impairment on some of these tests ð6Ł\ patients with frontal lobe lesions tend to be the most uniformly and severely impaired group across these various measures[

Subject groups] synopsis of quantitative MRI and PET _ndings Detailed quantitative MRI and PET _ndings will be pre! sented elsewhere[ The MRI|s have been segmented and analysed according to pre!determined structural de_nitions using a hier! archical segmentation programme ð02Ł\ which allows _ne!grai! ned measures of volume[ The PET analyses have been conducted in 5 di}erent ways*using absolute metabolism values\ standard uptake values and ECAT count ratios\ each of which has been analysed in terms of a region!of!interest "R!o!I# template and the SPM programme ð09Ł[ For present purposes\ we will simply report _ndings pertinent to identifying focal lesions\ atrophy\ or hypometabolism within each patient group[ For MRI\ the signi_cance values were calculated in terms of one!way ANOVAs across the 6 main diagnostic groups "con! trols\ Korsako}\ Pituitary irradiation\ herpes encephalitis\ hypoxia\ frontal tractotomy\ and frontal focal# with Duncan|s

Table 1[ Frontal lobe "{{executive||# test performance] mean scores "20 S[D[# across the 3 patient groups Healthy controls

FAS verbal ~uency "r  8Ð60# Card sorting categories "r  9Ð5# ) persev|ns "r  9Ð099# Cognitive estimates "r  9Ð04#

M

S[D[

39[2 4[9 02[0 2[8

202[6 20[5 203[6 21[6

 "Perseverative errors6Total errors#)[ r  range[

Frontal lobe patients M S[D[

Diencephalic patients M S[D[

Temporal lobe patients M S[D[

12[6 2[2 30[2 7[8

21[1 2[6 21[8 5[8

21[7 3[3 12[8 5[0

202[6 20[8 229[9 22[8

204[4 20[8 220[3 23[3

202[5 20[6 214[3 22[1

F

P

2[85 2[96 2[84 4[75

³9[90 ³9[94 ³9[90 ³9[990

) 677

M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory in varying sites "1 bilateral\ 2 right unilateral\ 0 left unilateral#[ On MRI\ this group did not di}er signi_cantly from healthy controls in terms of total brain volume^ but they did di}er signi_cantly "P ³ 9[94# when the lesion volume in the frontal lobes was subtracted to give brain minus lesion volume[ In terms of PET\ pooling the data from the left and right hemi! spheres\ the focal frontal group showed statistically signi_cant hypometabolism in the dorso!lateral and orbito!medial frontal lobes\ anterior cingulate and {{whole frontal lobes||[ In neither R!o!I nor SPM analysis was there statistically signi_cant hypo! metabolism elsewhere than in these frontal regions[ All 02 Korsako} patients showed evidence of thalamic atro! phy on MRI and as a group\ they di}ered signi_cantly "P ¾ 9[90# from the controls in this regard[ Nine out of 02 Korsako} patients also showed evidence of mammillary body atrophy[ These changes were symmetrical in 01 of the 02 pati! ents[ The remaining patient had a large left!sided thalamic infarct[ In terms of global brain volume\ there was indeed some degree of atrophy\ as would be expected in this group[ However\ on Duncan|s Multiple Range test\ this was signi_cant at only the P  9[94 level and it was mainly attributable to 1 individual patients[ After excluding these 1 patients\ the Korsako} group did not di}er signi_cantly from the healthy controls in terms of global atrophy[ However\ these 1 patients| performance on the tasks investigated in the present study was entirely typical of the rest of the Korsako} group[ On PET R!o!I analysis\ the Korsako} group did not di}er signi_cantly from the controls in any brain region[ On SPM\ they showed statistically signi_cant "P ³ 9[94# bilateral hypometabolism in the frontal poles\ mainly attributable to changes in 3 subjects only\ although these 3 subjects did not di}er from the rest of the group in terms of performance on frontal:executive tests[ Surprisingly little has emerged from the quantitative MRI and PET analyses of the two Pituitary irradiation patients to date and they did not di}er signi_cantly from the controls on

Multiple Range post!hoc tests "at P ¾ 9[94# to compare each patient group with the healthy control group\ unless otherwise speci_ed[ In the case of PET analyses\ statistical signi_cance for R!o!I has been determined similarly\ using one!way ANOVAs and Duncan|s Multiple Range post!hoc tests "P ³ 9[94#across the 6 main diagnostic groups[ The analysis reported is in terms of raw ECAT count ratios relative to occipital metabolism "there was no signi_cant di}erence across the groups in terms of occipital absolute metabolism#[ This measure was used as it maximised the sample size "some patients did not stay in the scanner long enough for absolute metabolism values to be obtained#[ The SPM programme is based on voxel! by!voxel t!test comparisons "between each patient group and the control group#] from this a statistical parametric map of Z values is generated\ which can be thresholded at a pre! determined level of statistical signi_cance "P ³ 9[90 in our analyses# ð09Ł[ The MRI and PET _ndings in the frontal tractotomy group\ obtained 1 weeks| post!operatively and within a day or two of cognitive testing\ were highly consistent from subject!to! subject[ Figure 0a shows the yttrium deposits on MRI bilat! erally\ surrounded by a sizeable area of irradiation necrosis which\ in turn\ is engulfed by a large area of oedema[ Figure 0b shows that this necrosis and oedema was accompanied by severe hypometabolism\ demonstrable on PET[ Interestingly\ there was a margin of cortical tissue apparently una}ected by the oedema\ which was found in all the individual subjects in this group and this was clearly visible on MRI "Fig[ 0#[ As expected\ there was no evidence of brain atrophy in this group on MRI[ On both PET measures "i[e[ R!o!I and SPM#\ this group showed statistically signi_cant hypometabolism in the dorso!lateral and orbito!medial frontal cortex\ in the anterior cingulate region\ as well as in the {{whole frontal lobe||[ There was no statistically signi_cant hypometabolism in any other brain region[ The focal frontal group had MRI!con_rmed frontal lesions

Fig[ 0[ Shows "i# MRI axial section and "ii# FDG!PET axial section from a typical patient 1 weeks| post!tractotomy[ The MRI shows the mid!frontal yttrium deposits bilaterally\ surrounded by an area of radiation necrosis and a much larger area of oedema "sparing the cortical margins#[ The PET shows a corresponding and extensive region of frontal hypometabolism[

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M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory any measure[ We are currently seeking to enlarge this sample to examine this group in more detail[ However\ an apparently normal MRI scan does not mean that the underlying tissue is normal ð16\ 36Ł[ By superimposing the irradiation _elds on these patients| MRI scans\ we can identify that the anterior thalamus\ fornix\ mammillo!thalamic tract and mammillary bodies were subjected to irradiation ð03Ł[ The fact that this irradiation was followed by a clinically and neuropsychologically severe ante! rograde memory disorder\ in the absence of any global cognitive impairment\ would appear to con_rm that there must be dam! age within these structures\ albeit at a microscopic level[ In the present study\ this group|s performance fell well within the range of the Korsako} group on the key outcome measures and did not di}er signi_cantly from the Korsako} means "recall! recognition] t  9[34 n[s[^ categorised!unrelated word recall^ t  9[53 n[s[#[ The herpes encephalitis group showed temporal lobe abnor! malities on MRI and PET clearly apparent to the naked eye in all cases[ In 7 out of 8 patients\ these were asymmetrical but\ despite this\ when the _ndings from the left and right hemi! sphere were pooled\ there were signi_cant abnormalities in tem! poral lobe volume and metabolism[ These included signi_cant reductions in total hippocampal "P ³ 9[94#\ parahippocampal "P ³ 9[94# and combined hippocampal and parahippocampal volumes "P ³ 9[90# on MRI[ In terms of PET R!o!I\ these patients showed statistically signi_cant hypometabolism in the medial\ inferior and anterior temporal regions\ but there was no signi_cant hypometabolism in any other brain region[ On SPM analysis\ the lateral temporal cortex was also implicated[ As mentioned above\ 2 of the 3 hypoxic patients had unequivocal CT scan evidence of temporal lobe changes\ when this was performed shortly after the cerebral insult and the remaining patient appeared to have bilateral temporal lobe hypometabolism on initial visual inspection of his PET[ The research MRI was usually carried out some months after the initial cerebral insult\ at which point the hypoxic group showed a signi_cant reduction in total hippocampal volume "t  1[06\ P  9[94#[ An unexpected additional _nding was that 2 of the 3 hypoxic patients showed thalamic hypometabolism on PET scan and this was statistically signi_cant on both R!o!I and SPM[ Clinically\ this is not altogether surprising\ since hypoxic patients sometimes show focal points of altered signal in sub! cortical grey matter\ evident on MRI or even CT scan[ However\ it was unexpected in view of the way these patients had been selected on clinical and CT evidence for inclusion in the study[ In brief\ there was evidence for both temporal lobe and thalamic changes in this group[ In the analyses below\ we have included the hypoxic patients in the temporal lobe group\ i[e[ in the manner in which they had been selected originally on the clinical and CT evidence[ It will be seen below that the temporal lobe group as a whole performed closely similarly to the diencephalic group and this remained true after exclusion of the hypoxic patients[ Consequently\ in some of the comparisons below\ we have chosen to combine the diencephalic and tem! poral lobe groups in order to contrast their performance with that of the frontal lobe group*hence\ the fact that 2 subjects in this group had evidence of pathological changes in both sites does not a}ect the overall conclusions\ drawn from these comparisons[

Materials Thirty!two words\ all 0 or 1 syllables long\ were selected[ Sixteen of the words were unrelated] the other 05 words fell into 1 categories\ 7 words in each\ taken from the Battig and Montague ð2Ł norms[ The mean word frequency of both the unrelated and categorised words was 017 occurrences per

678

million ð8Ł[ The 21 words were divided into 1 lists "A and B# of 05 words\ so that there were 7 unrelated words and 3 words from the 1 categories in each[ The 1 lists were matched for word frequency and syllable length[ Each word was typed on a 5ý×3ý ~ash card[ The words in each list were divided into 3 blocks\ 1 unrelated and 1 categor! ised[ The 3 blocks within each list were arranged so that unre! lated and categorised blocks alternated[ Each block of words was preceded by a card on which was written either {{unrelated||\ or the name of the category from which the words were taken[ The words within each block were presented in a di}erent random order for each subject\ and the presentation order of unrelated and categorised groups of words was rotated across subjects[ For the construction of a forced!choice recognition memory test\ the matched word list was employed[ Each {{target|| word was paired with a comparable word from the distractor list "i[e[ an unrelated target word was paired with an unrelated distractor word# and typed on a 5ý×3ý card[ Each list "i[e[ A and B# served equally often as targets and distractors within and across subject groups[

Procedure Subjects were presented with a word list consisting of 05 items\ consisting of 1 blocks of 3 categorised words and 1 blocks of unrelated words[ They were told that they would be shown a series of words and that they were to read each one aloud and to try to remember them[ They were told that the words would be divided into 3 blocks\ that in 1 of the blocks the words were unrelated to each other\ and that the words in the other 1 blocks came from 1 di}erent categories and were in some way related to one another[ Subjects were also told that before each block of words a card would be presented with either the word {{unre! lated|| written on it or the name of the category from which the words were taken[ Exposure times were varied across the di}erent subject groups in order to match group mean recognition memory scores as closely as possible[ At the start of the study\ exposure times for the subjects in each group were determined on the basis of _ndings from similar studies in the literature as well as some pre!study piloting[ However\ some occasional adjust! ments were required during the course of the experiment in order to optimise matching across the subject groups[ Once a subject had completed the experiment\ the mean recognition score in that subject|s group was recalculated\ and the exposure times to targets were occasionally adjusted for subsequent sub! jects in order to optimise matching of the group means for recognition memory[ The mean exposure time per word at the end of the experiment was 8[2 s for both the diencephalic and temporal lobe groups and 2[7 s and 2[1 s for the frontal lobe group and healthy controls respectively[ Mayes ð21\ 22Ł has pointed out that\ in studies in which memory!impaired patients have longer stimulus exposure times than controls\ the total duration of the presentation phase and mean item!to!test delay will be longer for patients[ As a result\ the patients| performance may be underestimated[ To overcome this problem\ we included an inter!stimulus task during pres! entation to match the total duration across the 3 groups over which the stimuli were presented[ Subjects where shown a card with a number between 099 and 0999 on it and were required to count backwards by 2|s until the next word was presented[ The length of time a subject was required to count was inversely proportional to the length of time the words were presented\ so that each item was presented 09 s after the previous item had _rst appeared[ For example\ if the targets were studied for 4 s each\ the subtraction task lasted 4 s^ if the targets were studied for 3 s\ subtraction was adjusted to last 5 s[ All subjects per!

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M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

formed the inter!stimulus task except those who were shown the words for the maximum time of 09 s each[ Following pres! entation of the last word\ all subjects counted backwards for 14 s until the instructions for the free recall test were given[ After 29 s delay\ memory testing commenced[ As in the Hirst et al[ ð06\ 07Ł and Janowsky et al[ ð19Ł studies\ recognition memory was tested following completion of recall testing on the same material] subjects were given a free recall task\ a cued recall task and then a forced!choice recognition memory task[ During the free recall test\ subjects were asked to recall as many words as possible in any order^ when it was clear that no more words could be retrieved\ subjects were given the cued recall task[ In this\ subjects were given the category names and reminded that some of the words were unrelated^ but\ because the results for cued recall did not di}er essentially from those for free recall\ they will not be presented here[ Finally\ subjects were given the recognition test in which they were asked which of 1 words "from the matched lists described under {{Materials||# they had originally seen[

Results Despite our titrating exposure times in this task\ we found that a number of subjects scored at ceiling on recognition memory[ Consequently\ the data are pre! sented in two ways[ First\ we excluded all subjects who scored at ceiling "05 words correct# on the recognition memory test] this left 03 controls\ 7 frontal lobe patients\ 03 diencephalic patients and 00 temporal lobe patients[ Secondly\ we examined our data for all subjects\ including those who scored at ceiling on recognition[ As will be seen below\ the _ndings were highly consistent[ Figure 1a shows recognition memory performance and free recall scores in the {{matched|| groups "excluding subjects at ceiling# and Fig[ 1b shows the same analysis for all subjects[ In Fig[ 1a\ there was no signi_cant di}er!

ence across the groups in terms of recognition memory scores\ "F"2\32#  0[74\ n[s[#[ In the total group "Fig[ 1b#\ there was a signi_cant di}erence in recognition scores "F"2\32#  2[24^ P ³ 9[914#\ accounted for by the superior performance of the control and frontal lobe patient groups[ However\ the important point was that\ when recognition and free recall were compared\ the curves remained in parallel] neither the frontal lobe group nor the amnesic "diencephahlic and temporal lobe# pat! ients showed a disproportionate impairment on recall memory relative to controls[ This was analysed using "recognition minus free recall# di}erence scores[ For the matched sub!groups\ there was no signi_cant di}erence across the subject groups in terms of di}erence scores "F"2\32#  9[53\ n[s[#[ There was also no signi_cant di}erence in "recognition minus recall# di}erence scores across the total groups "F"2\59#  9[47\ n[s[#[ As a double! check\ we also compared the groups in pairs in terms of recognition!recall di}erence scores\ using conventional unmatched t!tests] none of the t!tests approached stat! istical signi_cance[ This _nding cannot be attributed to a {{~oor|| e}ect in our patient groups for free recall\ as they were scoring approximately 29) correct on free recall\ compared with scores less than 09) in Hirst et al[|s ð06Ł and Haist et al[|s ð05Ł studies[ Figure 2a shows percent correct for unrelated items and {{blocked|| categorised items within the free recall task for the same matched sub!groups as before[ Figure 2b shows the equivalent _ndings for the total subject groups[ In both _gures\ it can be seen that all groups bene_ted from {{blocked|| categorisation\ but the control group and the frontal lobe group appear to have bene_ted di}erentially more than the diencephalic and temporal lobe amnesic patients[ Within the selected subgroups

Fig[ 1[ Recognition and free recall performance across the 3 lesion groups "a# for the {{matched|| samples in which subjects at ceiling were excluded\ and the groups did not di}er signi_cantly in terms of recognition memory scores^ and "b# for the total "unselected# samples\ in which there was a signi_cant di}erence in recognition memory scores across the groups[

M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

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Fig[ 2[ Free recall performance across the 3 lesion groups showing the _ndings for "i# unrelated words^ and "ii# words {{blocked|| into groups by semantic categories[ Figure 2a shows the _ndings for the samples {{matched|| in terms of recognition memory performance^ and Fig[ 2b shows the _ndings for the total "unselected# samples[

"Fig[ 2a# there was actually a crossover\ whereby the frontal lobe group did worse than the diencephalic and temporal lobe amnesic patients on unrelated words\ but better than the amnesic patients on categorised words[ Analysing these results in terms of "categorised minus unrelated# di}erence scores\ and on the basis of the hypothesis that the control and frontal groups should show a di}erential bene_t from semantic categorisation\ there was a signi_cant di}erence across the groups "F"2\ 32#  1[21^ P ³ 9[94\ 0 tailed#[ Moreover\ in terms of unmatched t!test comparisons\ the control and frontal groups di}ered signi_cantly from the combined "dien! cephalic and temporal lobe# amnesic groups "t  1[48\ P ³ 9[904# and the frontal lobe group alone also di}ered signi_cantly from the 1 combined amnesic groups "t  1[19\ P ³ 9[94# and from the diencephalic group taken in isolation "t  1[09\ P ³ 9[94#[ Examining the data from the total subject groups "Fig[ 2b#\ in terms of "categorised minus unrelated# di}erence scores\ the groups showed only a trend towards statistical sig! ni_cance "F"2\59#  0[56^ P ³ 9[09\ 0!tailed#[ However\ in terms of individual t!test comparisons\ the control and frontal groups showed signi_cantly larger di}erence scores than the combined diencephalic and temporal lobe groups "t  1[05\ P ³ 9[94#[ Moreover\ the frontal group alone also showed signi_cantly larger di}erence scores than the combined "diencephalic and temporal lobe# amnesic groups "t  0[78\ P ³ 9[94\ 0 tailed# and than the temporal lobe group taken in isolation "t  0[66\ P ³ 9[94\ 0 tailed#[ Taken together\ these _ndings indi! cate that the frontal lobe group could bene_t from the semantic categorisation of words to a signi_cantly greater degree than the diencephalic or temporal lobe amnesic patients[

On the other hand\ there were only minimal categorised minus unrelated word di}erences within groups on the recognition memory task\ and no signi_cant di}erences across the groups[ In order to examine the relationship between recall and recognition memory and executive or frontal lobe function in further detail\ we compared correlations between performance on our tasks with memory quo! tients "GMQ\ DMQ#\ on the one hand\ and fron! tal:executive task performance on the other[ We hypothesised that if frontal lobe function were par! ticularly crucial for recall memory\ correlations with frontal:executive tests would be greater for our recall than our recognition measures[ Within the total patient group "frontal\ diencephalic\ and temporal lobe#\ word recall scores correlated signi_cantly with WMS!R GMQ "r  9[65\ P ³ 9[9990# and DMQ "r  9[52\ P ³ 9[9990#[ Similarly\ word recognition scores correlated signi_! cantly\ although to a slightly smaller extent\ with these 1 measures "r  9[41\ P ³ 9[990^ and r  9[39\ P ³ 9[90\ respectively#\ re~ecting the fact that the WMS!R is itself predominantly a recall memory measure[ On the other hand\ across the total patient group\ correlations with measures of frontal:executive function "FAS verbal ~u! ency\ card!sorting categories and percentage persever! ations\ and cognitive estimates| score# were relatively low\ statistically non!signi_cant\ and comparable between the word recall and recognition measures[ In fact\ the only correlation with frontal:executive function which approached statistical signi_cance was that between card!sorting categories and word recognition memory "r  9[17\ P ³ 9[96#[ In brief\ the absence of any speci_c correlation between word recall memory and frontal: executive function _ts with the main _nding that frontal

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M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

lobe lesions do not produce a disproportionate impair! ment in recall memory[ In order to examine whether initial di}erences in mean IQ minus GMQ scores had in~uenced the results "the frontal group were less severely amnesic*see Table 0#\ we correlated the recognition minus free recall di}erence score with IQ minus GMQ across the total patient group "n  33#[ The correlation was only 9[06 "n[s[#\ and the corresponding correlation for IQ minus DMQ was 9[98 "n[s[#[ The correlations with NART!R minus GMQ and NART!R minus DMQ were also non!signi_cant\ indi! cating that IQ!MQ di}erences had not in~uenced the overall result[ We also examined for di}erences between 6 aeti! ological groups "Korsako} syndrome\ pituitary irradiation\ herpes encephalitis\ anoxic:epileptic tem! poral lobe damage\ frontal tractotomy\ focal frontal lesions and healthy controls#[ The _ndings for recall: recognition di}erences are shown in Figs 3a and 3b[ Although there was a weak trend for the anoxia:epilepsy group "3 hypoxic patients and 0 epileptic patient with mesial temporal sclerosis# to show the largest discrep! ancy\ there were no signi_cant di}erences in recognition minus free recall scores across either the matched sub! groups "F"5\39#  0[26\ n[s[# or the total subject groups "F"5\46#  9[72\ n[s[#\ the performance of the other groups closely resembling one another[ On the other hand\ consistent with the _ndings for the main lesion groups\ di}erence scores between categorised and unre! lated words in free recall showed signi_cant di}erences across the matched subgroups "F"5\39#  1[49\ P ³ 9[94# and just failed to reach statistical signi_cance across the total groups "F"5\ 46#  1[95\ P ³ 9[964Ł[ In this case\ the two frontal groups showed the greatest bene_t from

semantic categorisation "Fig[ 2# and the anoxic:epileptic\ Pituitary and Korsako} groups showed the least bene_t[ As previous studies have suggested that there might be variability between frontal lobe patients in terms of disproportionate impairment for recall or recognition\ we made a speci_c comparison of the frontal tractotomy "n  8# vs focal frontal lesions "n  5# for recognition minus recall di}erence scores "M  6[98 "21[36# and 5[54 "22[21# respectively] t  9[18\ n[s[#[ We carried out the same comparison for categorised minus unrelated di}erence scores in the free recall condition "M  31[8 "229[5# and 26[2 "216[2# respectively# and again this was not statistically signi_cant "t  9[25\ n[s[#\ indicating that the performance of these 1 frontal groups closely resembled each other[ Because a parallel study on tem! poral context memory ð29Ł had suggested that 2 patients with lesions penetrating the dorso!lateral frontal cortex behaved di}erently from patients with more medial fron! tal lesions\ we also compared these 2 patients with the rest of the frontal lobe group\ again _nding no signi_cant di}erences in terms of either recognition minus recall or categorised minus unrelated words "within the free recall condition#[

Discussion This is a topic on which the previous literature has produced some disparate _ndings[ On the one hand\ some authors ð19\ 31Ł have argued that patients with frontal lobe lesions show a disproportionate impairment on recall memory\ whilst 2 studies have drawn attention to patients with frontal lobe lesions who performed par! ticularly badly on recognition memory measures ð5\ 11\

Fig[ 3[ Recognition and free recall performance across the 6 diagnostic groups show _ndings for "a# the {{matched|| samples in which subjects at ceiling were excluded and "b# for the total "unselected# samples[

M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

39Ł[ The Kartsounis et al[ ð11Ł study involved di}erent frontal tractotomy patients from the same source as our own\ although their study did not attempt to match levels of either recall or recognition memory performance[ Indeed\ in both the Delbecq!Derouesne et al[ ð5Ł and the Kartsounis et al[ ð11Ł studies\ di}ering measures were used for assessing recall and recognition memory and\ in addition\ intrusion errors:false positives may have been penalised in di}erent ways across their tasks[ By contrast\ Hirst et al[ ð06\ 07Ł have argued that there is a dis! proportionate impairment in recall memory by amnesic patients in general\ although others have disputed this ð05Ł[ Aggleton and Shaw ð0Ł have argued\ on the basis of a meta!analysis\ that lesions in the hippocampus\ fornix\ or mammillary bodies a}ect recall but not recognition\ whereas larger lesions or lesions elsewhere impair rec! ognition memory as well] however\ no neuro!imaging data were presented in their study and the quality of the localisation data in the studies they cite is immensely variable[ In short\ the status of recall and recognition memory in organic amnesia and frontal lobe pathology has remained very unclear[ This partly results from the di.culty in avoiding ceiling and ~oor e}ects in such studies and from the varying techniques which have been used to {{match|| either recognition or recall in di}erent investigations[ In the present study\ we manipulated the exposure time of word stimuli in order to match recognition scores as closely as possible and we also equated the total duration over which the stimuli were presented to the di}erent groups[ Despite this procedure\ we still obtained ceiling e}ects in some of our subjects\ but comparison of the results in selected sub!groups\ in whom ceiling e}ects had been avoided\ with _ndings from the total groups gave very consistent results across all analyses[ A potential criticism is that we tested recall and recognition in suc! cession on the same word lists[ However\ this design was based on that employed by both Hirst et al[ ð06\ 07Ł\ who studied amnesic patients\ and Janowsky et al[ ð19Ł\ who investigated patients with frontal lesions] yet we obtained very di}erent _ndings from both of those groups[ Hence\ the discrepancy in the results cannot be attributed to this aspect of the design[ In our study\ unlike theirs\ there was no evidence of a disproportionate impairment in recall memory\ relative to recognition memory\ in either the frontal lobe or the amnesic "diencephalic and temporal lobe# groups[ Moreover\ this general conclusion also applied when comparison was made across the under! lying diagnostic or aetiological groups[ Other studies have also investigated groups of patients with varying underlying diagnoses\ although the performance of their subgroups has not always been reported[ Hirst et al[ ð06Ł examined 6 non!Korsako} patients of varying aetiology and 8 Korsako} amnesic patients[ Hirst et al[ ð07Ł studied 5 patients varying in aetiology[ Janowsky et al[ ð19Ł stud! ied 6 frontal patients of very varying aetiology\ 6 Kor! sako} patients and 4 other amnesic patients\ again of mixed aetiology[ Delbecq!Derousne et al[ ð5Ł studied a

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single case[ Haist et al[ ð05Ł investigated 01 patients with Korsako}|s syndrome and 5 other amnesic patients of various aetiologies[ Even in a meta!analysis\ Aggleton and Shaw ð0Ł based their conclusions about hippocampal lesions on only 6 subjects\ who consisted of 1 patients with fornix lesions\ 2 with hippocampal ischaemia and 1 with mammillary body damage[ By comparison\ our study included 02 Korsako} patients\ 8 herpes encepha! litis\ 8 frontal tractotomy and 5 focal frontal lesions\ the pattern of performance being highly consistent across these groups in terms of the absence of any recall!rec! ognition discrepancy[ The Janowsky et al[ ð19Ł study was confounded by a ceiling e}ect\ and there may be a fairly simple explanation for the apparent di}erence in our result from Hirst et al[|s ð06\ 07Ł _ndings[ We chose a 29 s delay following presentation of the stimuli\ because we were anxious to avoid ~oor e}ects in the free recall task and because we assumed that this was the minimum delay which would avoid confounding the results with e}ects from {{working memory|| ð1\ 14Ł[ Hirst et al[ ð07Ł had used 29 s as the test delay for amnesic patients in their Experiment 0\ in which these patients were compared with controls tested at a 13 h delay[ On the other hand\ Hirst et al[|s ð06\ 07Ł two other experiments\ in which the exposure time to target stimuli had been titrated "as in the present study#\ used test delays of 4 min and 1 min respectively[ Our own forgetting rate studies ð18Ł have found normal verbal and non!verbal short!term forgetting in amnesic patients\ but we have also shown that these same groups of dien! cephalic and temporal lobe amnesic patients forgot faster on free recall tasks between delays of 19Ð14 s and 09 min ð01\ 18Ł[ In these studies\ the frontal group showed only a weak "non!signi_cant# trend in the direction of faster forgetting on recall tasks[ However\ on recognition memory\ there were no di}erences in forgetting rates in any of the groups at any delays[ Consequently\ the prediction from our forgetting studies would be that in diencephalic and temporal lobe amnesic patients\ but not necessarily in patients with frontal lobe lesions\ a recall:recognition di}erence would emerge at delays longer than 29 s\ as Hirst et al[ ð06\ 07Ł found[ Against this\ Haist et al[ ð05Ł have failed to _nd any delay!dependent di}erences in recall:recognition performance[ We plan future studies to investigate this issue further[ The one di}erence between the patient groups\ which emerged in our present study\ was that the frontal lobe patients di}ered from the 1 amnesic "diencephalic and temporal lobe# groups in showing a di}erential bene_t from the cues provided by semantic organisation[ In a comparable study examining list learning for unrelated words as well as {{unblocked|| and {{blocked|| sem! antically categorised words\ Stuss et al[ ð33Ł failed to _nd any di}erential bene_t from semantic categorisation in frontal lobe lesion patients\ relative to healthy controls[ However\ there were 1 main di}erences in that inves! tigation from the present study] "i# the present study manipulated exposure times\ and it may be that pro!

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longed exposure is necessary for the frontal lobe patients to be able to make use of semantic cues^ and "ii# the di}erential bene_t from semantic organisation in the pre! sent study was particularly evident in comparison with the diencephalic and temporal lobe amnesic patients "who were impaired in this respect#\ rather than in comparison with healthy controls[ It is also\ of course\ plausible that there may have been di}erences relating to the underlying aetiologies of the lesions across the 1 studies "although these did not appear important within the present study# or in the extent of non!frontal involvement[ A disproportionate impairment in recall memory was used by Hirst et al[ ð06\ 07Ł to argue for a de_cit in contextual encoding as an important factor underlying amnesic patients| memory impairment[ In other studies\ we have found speci_c contextual memory de_cits in diencephalic and temporal lobe amnesic patients ð12\ 29Ł] the present _nding would suggest that these contextual memory de_cits do not have speci_c e}ects upon recall "as opposed to recognition# memory at encoding:acquisition\ although it is still possible that they may have speci_c consequences upon the retention of recalled information ð01Ł[ On the other hand\ Shimamura et al[ ð19\ 31Ł and Delbecq!Derouesne et al[ ð5Ł have argued from opposing points!of!view that speci_c recall:recognition de_cits imply that the memory disorder in patients with frontal lobe lesions di}ers qualitatively from that seen in "dien! cephalic:temporal lobe# amnesic patients[ After matching our groups as closely as possible on a recognition measure\ we failed to _nd a disproportionate de_cit in the frontal lesion patients in recall memory[ However\ we did _nd a subtler manner in which they were di}er! entiated from other amnesic patients\ namely in their ability to respond to the cues provided by semantic organ! isation[ This might be interpreted as implying that\ com! pared with the "diencephalic and temporal lobe# amnesic groups\ theirs is more a de_cit in retrieval or access\ rather than storage[ Alternatively\ the frontal lobe patients may have particular di.culty in organising spontaneously their learning of unrelated words\ compared with healthy controls[ It may well be the case that frontal patients exist who show speci_c or disproportionate impairments in either recall or recognition\ whether as the extremes of a continuum or in relation to speci_c sites of focal lesion\ but we were unable to identify such cases in the present sample[ Acknowled`ements*This research was funded by a Wellcome Trust grant awarded by Drs M[ D[ Kopelman\ J[ Wade and B[ Kendell[ We would like to thank Elizabeth Guinan for help with testing subjects[

References 0[ Aggleton\ J[ P[ and Shaw\ C[\ Amnesia and rec! ognition memory] a re!analysis of psychometric data[ Neuropsychologia\ 0885\ 23\ 40Ð51[

1[ Baddeley\ A[ D[\ Human Memory] Theory and Prac! tice[ Lawrence Erlbaum Associates\ Hove and London\ 0889[ 2[ Battig\ W[ F[ and Montague\ W[ E[\ Category norms for verbal items in 45 categories[ Journal of Exper! imental Psycholo`y\ Mono`raph\ 0858\ 79\ 0Ð35[ 3[ Benton\ A[ L[\ Di}erential behavioral e}ects of fron! tal lobe disease[ Neuropsycholo`ia\ 0857\ 5\ 42Ð59[ 4[ Butters\ N[\ Salmon\ D[ P[\ Munro Cullum\ C[\ Cairns\ P[\ Troster\ A[ I[ and Jacobs\ D[\ Di}er! entiation of amnesic and demented patients with the Wechsler Memory Scale*Revised[ The Clinical Neu! ropsycholo`ist\ 0877\ 1\ 022Ð037[ 5[ Delbecq!Derouesne\ J[\ Beauvois\ M[ F[\ and Shal! lice\ T[\ Preserved recall versus impaired recognition[ Brain\ 0889\ 002\ 0934Ð0963[ 6[ Corcoran\ R[ and Upton\ P[\ A role for the hip! pocampus in card sording< Cortex\ 0882\ 18\ 182Ð 293[ 7[ Cutting\ J[\ The relationship between Korsako}|s syndrome and alcoholic dementia[ British Journal of Psychiatry\ 0867\ 021\ 139Ð140[ 8[ Francis\ W[ N[ and Kucera\ H[\ Frequency Analysis of En`lish Usa`e] Lexicon and Grammar[ Boston\ Houghton Mi/in Co[\ 0871[ 09[ Friston\ K[ J[\ Frith\ C[ D[\ Liddle\ P[ F[ and Frackowiak\ R[ S[ J[\ Comparing functional "PET# images] the assessment of signi_cant change[ Journal of Cerebral Blood Flow and Metabolism\ 0880\ 00\ 589Ð588[ 00[ Grasby\ P[ M[\ Frith\ C[ D[\ Friston\ K[ J[\ Bench\ C[\ Frackowiak\ R[ S[ and Dolan\ R[ J[\ Functional mapping of brain areas implicated in auditory!verbal memory function[ Brain\ 0882\ 005\ 0Ð19[ 01[ Green\ R[ E[ A[ and Kopelman\ M[ D[\ Contribution of context!dependent memory and familiarity judge! ments to forgetting rates in organic amnesia[ Sub! mitted for publication[ 02[ Gri.n\ L[ D[\ Colchester\ A[ C[ F[\ Rollsa\ S[ A[\ Studholm\ C[\ Hierarchical segmentation tool satisfying constraints[ In Proceedin`s of the British Machine and Vision Conference\ ed[ E[ R[ Hancock[ BNVA Press\ She.eld\ 0883\ pp[ 024Ð033[ 03[ Guinan\ E[ M[\ Kopelman\ M[ D[\ Stanhope\ N[\ Lewis\ P[ and Lowy\ C[\ The cognitive e}ects of pituitary tumours and their treatments] 1 case studies and an investigation of 89 patients[ Journal of Neuro! lo`y\ Neurosur`ery\ and Psychiatry\ in press[ 04[ Hamilton\ M[\ Development of a rating scale for primary depressive illness[ British Journal of Social and Clinical Psycholo`y\ 0856\ 5\ 167Ð185[ 05[ Haist\ F[\ Shimamura\ A[ P[ and Squire\ L[ R[\ On the relationship between recall and recognition memory[ Journal of Experimental Psycholo`y] Learnin`\ Mem! ory and Co`nition\ 0881\ 07\ 580Ð691[ 06[ Hirst\ W[\ Johnson\ M[ K[\ Kim\ J[ K[\ Hirst\ W[\ Johnson\ M[ K[\ Phils\ E[ A[\ Risse\ G[ and Volpe\ B[ T[\ Recognition and recall in amnesics[ Journal of Experimental Psycholo`y] Learnin` Memory and Co`nition\ 0875\ 01\ 334Ð338[ 07[ Hirst\ W[\ Johnson\ M[ K[\ Phelps\ E[ A[ and Volpe\ B[ T[\ More on recognition and recall in amnesics[ Journal of Experimental Psycholo`y\ Learnin`\ Mem! ory and Co`nition\ 0877\ 03\ 647Ð651[

M[ D[ Kopelman and N[ Stanhope:Recall and recognition memory

08[ Jacoby\ L[ L[ and Kelley\ C[\ Unconscious in~uences of memory] dissociations and automaticity[ In The Neuropsycholo`y of Consciousness\ eds D[ Milner and M[ D[ Rugg[ Academic Press\ London\ 0881\ pp[ 190Ð122[ 19[ Janowsky\ J[ S[\ Shimamura\ A[ P[\ Kritchevsky\ M[ and Squire\ L[ R[\ Cognitive impairment following frontal lobe damage and its relevance to human amnesia[ Behavioral Neuroscience\ 0878\ 092\ 437Ð 459[ 10[ Kapur\ S[\ Craik\ F[ I[ M[\ Tulving\ E[\ Wilson\ A[ A[\ Houle\ S[ and Brown\ G[ M[\ Neuroanatomical correlates of encoding in episodic memory] levels of processing e}ect[ Proceedin`s of the National Acad! emy of Science\ USA\ 0883\ 80\ 1997Ð1900[ 11[ Kartsounis L[ D[\ Poynton\ A\ Bridges\ P[ K[ and Bartlett\ F[ R[\ Neuropsychological correlates of stereotactic subcaudate surgery[ Brain\ 0880\ 003\ 1546Ð1562[ 12[ Kopelman\ M[ D[\ Remote and autobiographical memory\ temporal context memory\ and frontal atrophy in Korsako} and Alzheimer patients[ Neu! ropsycholo`ia\ 0878\ 16\ 326Ð359[ 13[ Kopelman\ M[ D[\ Frontal lobe dysfunction and memory de_cits in the alcoholic Korsako} syndrome and Alzheimer!type dementia[ Brain\ 0880\ 003\ 006Ð 026[ 14[ Kopelman\ M[ D[\ Working memory in the amnesic syndrome and degenerative dementia[ Neur! opsycholo`y\ 0883\ 7\ 444Ð451[ 15[ Kopelman\ M[ D[\ The Korsako} syndrome[ British Journal of Psychiatry\ 0884\ 055\ 043Ð062[ 16[ Kopelman\ M[ D[\ What|s wrong and what|s right in neuropsychology and neuropsychiatry[ Co`nitive Neuropsychiatry\ 0885\ 0\ 164Ð177\ 0885[ 17[ Kopelman\ M[ D[ and Stanhope\ N[\ Subjective memory evaluations in patients with focal frontal\ diencephalic and temporal lobe lesions[ Cortex\ in press[ 18[ Kopelman\ M[ D[ and Stanhope\ N[\ Rates of for! getting in organic amnesia following temporal lobe\ diencephalic\ or frontal lobe lesions[ Neur! opsycholo`y\ 0886\ 00\ 232Ð245[ 29[ Kopelman\ M[ D[ Stanhope\ N[ and Kingsley\ D[\ Memory for temporal and spatial context in patients with focal diencephalic\ temporal lobe\ and frontal lobe lesions[ Neuropsycholo`ia\ 0886\ 24\ 0422Ð0434[ 20[ Kopelman\ M[ D[\ Stanhope\ N[ and Kingsley\ D[\ Retrograde amnesia in patients with focal di! encephalic\ temporal lobe or frontal lesions[ Sub! mitted for publication[ 21[ Mayes\ A[ R[\ Learning and memory disorders and their assessment[ Neuropsycholo`ia\ 0875\ 13\ 14Ð49[ 22[ Mayes\ A[ R[\ Human Or`anic Memory Disorders[ Cambridge\ Cambridge University Press\ 0877[ 23[ Mayes\ A[ R[\ Automatic memory processes in amnesia] how are they mediated< In The Neuro!

24[ 25[ 26[ 27[

28[ 39[

30[

31[

32[

33[

34[

35[ 36[

37[

684

psycholo`y of Consciousness\ eds A[ D[ Milner and M[ D[ Rugg[ Academic Press\ London\ 0881\ pp[ 124Ð151[ Mayes\ A[ R[ and Downes\ J[ J[\ What do theories of the functional de_cit"s# underlying amnesia have to explain< Memory\ 0886\ 4\ 2Ð25[ Nelson\ H[ E[\ A modi_ed card!sorting test sensitive to frontal lobe de_cits[ Cortex\ 0865\ 01\ 202Ð213[ Nelson\ H[ E\ and Willison\ J[ R[\ The National Adult Readin` Test\ Second Edition[ NFER!Nelson\ Wind! sor\ 0880[ Poynton\ A[ M[\ Kartsounis\ L[ D[\ Bridges\ P[ K[\ A prospective clinical study of stereotactic subcaudate tractotomy[ Psycholo`ical Medicine\ 0884\ 14\ 652Ð 669[ Shallice\ T[ and Evans\ M[ E[\ The involvement of the frontal lobes in cognitive estimates[ Cortex\ 0867\ 03\ 183Ð292[ Schacter\ D[ L[\ Curran\ T[\ Galluccio\ L[\ Milberg\ W[ P[ and Bates\ J[ L[\ False recognition and the right frontal lobe] a case study[ Neuropsycholo`ia\ 0885\ 23\ 682Ð797[ Shimamura\ A[ P[\ "0883# Memory and frontal lobe function[ In The Co`nitive Neurosciences\ ed[ M[ S[ Gazzaniga[ MIT Press\ Cambridge MA\ 0883\ pp[ 792Ð702[ Shimamura\ A[ P[\ Janowsky\ J[ S[ and Squire\ L[ R[\ What is the role of frontal lobe damage in memory disorders< In Frontal Lobe Function and Dysfunction\ eds H[ S[ Levin\ H[ M[ Eisenberg and A[ L[ Benton[ Oxford University Press\ 0880\ pp[ 062Ð084[ Stuss\ D[ T[\ Eskes\ G[ A[ and Foster\ J[ K[\ Exper! imental neuropsychological studies of frontal lobe functions[ In Handbook of Neuropsycholo`y\ eds F[ Boller and J[ Grafman\ Vol[ 8[ Elsevier Science BV\ 0883\ pp[ 62Ð084[ Stuss\ D[ T[\ Alexander\ M[ P[\ Palumbo\ C[ L[\ Buckle\ L[\ Sayer\ L[ and Pogue\ J[\ Organizational strategies of patients with unilateral or bilateral fron! tal lobe injury in word list learning tasks[ Neuro! psycholo`y\ 0883\ 7\ 244Ð262[ Tulving\ E[\ Kapur\ S[\ Markowitsch\ H[ J[\ Craik\ F[ I[\ Habib\ R[ and Houle\ S[\ Neuroanatomical correlates of retrieval in episodic memory\ auditory sentence recognition[ Proceedin`s of the National Academy of Science of the United States of America\ 0883\ 80\ 1901Ð1904[ Victor\ M[\ Adams\ R[ D[ and Collins\ G[ H[\ The Wernicke!Korsakoff Syndrome\ 0st edition[ F[ A[ Davis Co[\ Philadelphia\ 0860[ Von Cramon\ D[ Y[ and Markowitsch\ H[ J[\ The problem of localising memory in focal cerebro! vascular lesions[ In Neuropsycholo`y of Memory\ 1nd edn\ eds L[ R[ Squire and N[ Butters[ Guilford Press\ New York[ 0881\ pp[ 84Ð094[ Wechsler\ D[\ Wechsler Adult Intelli`ence ScaleÐ Revised[ Psychological Corporation\ London and New York\ 0870[

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Erratum Temporal and spatial context memory in patients with focal frontal\ temporal lobe\ and diencephalic lesions\ by M[ D[ Kopelman\ N[ Stanhope and D[ Kingsley\ Neuropsycholo`ia\ Vol[ 24\ No[ 01\ pp[ 0422Ð0434\ 0886[ The publisher regrets that two errors arose in the above printed article[ In the Abstract\ it was stated that there was {{a weak association with one frontal:executive task "card!sorting preservations#||[ This should have read {{a weak associ! ation in the frontal group with one frontal:executive task [ [ [||[ Secondly\ references 23 and 24 were cited in the wrong order\ reference 23 should have read {{Neuropsycholo`ia\ in press||\ and reference 24\ {{submitted for publication||[