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Journal of Neuropsychology (2015), 9, 137–156 © 2014 The British Psychological Society www.wileyonlinelibrary.com

Memory for between-list and within-list information in amnesic patients with temporal lobe and diencephalic lesions Nicola M. Hunkin1*, Mohammed Awad2 and Andrew R. Mayes3 1

Department of Psychology, University of Sheffield, UK Department of Neurosurgery, Charing Cross Hospital, London, UK 3 School of Psychological Sciences, University of Manchester, UK 2

Patients with medial temporal lobe damage and diencephalic damage were compared on two tests of verbal temporal order memory: between-list discrimination and within-list discrimination. Both patient groups were impaired relative to a group of healthy control participants. In addition, despite comparable levels of item recognition, the diencephalic group was impaired relative to the medial temporal lobe group on both within-list and between-list discrimination. Temporal order memory for between-list information showed a significant correlation with a composite measure of recognition memory, and the results are discussed in terms of the patients’ reliance on familiarity and distancebased processes to make temporal order judgments.

It is well established that amnesic patients demonstrate an impairment in memory for associative information (Mayes, Montaldi, & Migo, 2007). This may include information about the temporal or spatial context of an event (Kopelman, Stanhope, & Kingsley, 1997), the source of a target item (Gold et al., 2006), or the modality in which it is presented (Pickering, Mayes, & Fairbairn, 1989). Several studies have focused on the retrieval of temporal order or position information. These studies have consistently found that amnesic patients are impaired relative to normal healthy volunteers on a range of measures of temporal order memory: list discrimination (Downes, Mayes, MacDonald, & Hunkin, 2002; Hunkin, Parkin, & Longmore, 1994; Kopelman et al., 1997), judgments of recency (Huppert & Piercy, 1978; Meudell, Mayes, Ostergaard, & Pickering, 1985; Shaw & Aggleton, 1995), judgments of frequency (Huppert & Piercy, 1978; Meudell et al., 1985), and the recall and recognition of temporal order information (Mayes et al., 2001; Shimamura, Janowsky, & Squire, 1990). These studies have often found that, in amnesic patients, temporal order memory is more impaired than item recognition memory, particularly when brain damage is relatively selectively confined to structures such as the hippocampus (Mayes et al., 2001). The brain damage and functional disruption that underlies impaired temporal order memory in amnesics, however, is still not fully understood. With respect to the critical underlying brain damage, two regions have been implicated. One region, damage to any

*Correspondence should be addressed to Nicola M. Hunkin, Department of Psychology, University of Sheffield, Western Bank, Sheffield S10 2TP, UK (email: [email protected]). DOI:10.1111/jnp.12040

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part of which is believed to underlie impairments in temporal order memory, is a hippocampal system that minimally comprises the hippocampus, fornix and anterior thalamus (Aggleton & Brown, 1999). Damage to this system is an agreed cause of amnesia and is known to result in impairment on measures of associative memory, including temporal order memory. Another region that is believed to play a key role in many kinds of associative memory, including temporal order memory, is the pre-frontal cortex (PFC). Not surprisingly, patients with frontal lobe lesions also show impairments on measures of temporal memory (Duarte, Henson, Knight, Emery, & Graham, 2010; Mangels, 1997; Milner, Corsi, & Leonard, 1991; Shimamura et al., 1990). The amnesic patients who have been included in previous studies of temporal order memory, frequently have had aetiologies that include encephalitis, Wernicke-Korsakoff Syndrome (WKS) and closed head injury. The pathology in these patients is likely to include frontal lobe pathology. Thus, frontal lobe dysfunction may contribute to amnesic patients’ difficulties in remembering temporal order information, although it has been argued that frontal lobe damage is not a pre-requisite for a deficit in this kind of memory (Parkin & Hunkin, 1993; Parkin, Rees, Hunkin, & Rose, 1994; see also Shuren, Jacobs, & Heilman, 1997). Consistent with this argument, there was no evidence that the hippocampal patient, YR, who showed several kinds of impaired temporal order memory, had PFC damage (Mayes et al., 2001). What functional deficits, likely to cause problems in temporal order memory, could be predicted to arise following damage to the hippocampal system and to the PFC respectively? Damage to the hippocampal system is believed by many (e.g., Aggleton & Brown, 1999) to disrupt long-term memory storage of associative information of the kind that must include the information necessary to support temporal order memory. To the extent that this kind of deficit underlies the problem, one might particularly expect that the severity of temporal order memory deficits should correlate with the severity of free recall deficits, which are always associative. In contrast, PFC damage is believed to disrupt executive functions such that the strategic aspects of encoding and retrieval will be impaired. This will inevitably affect the ability to use the kinds of associative information that are needed to support temporal order memory. To the extent that dysexecutive problems underlie patients’ temporal order memory deficits, these two kinds of deficit should be correlated with each other. However, few theories of how temporal order memory works have been developed and it remains unclear whether different theories are needed to explain different kinds of temporal order memory. Friedman (2001) has outlined two types of theory: ‘locationbased’ and ‘distance-based’. According to location-based theories, the ability to retrieve temporal information relies upon the relationship between the target event and some specific, unchanging source of temporal information. Friedman argues that the most successful location-based theories are reconstructive theories in which the timing of an event is judged by relating available information about that event to stored knowledge about personal, natural or social time patterns. For example, in recalling a visit to the Natural History Museum, I remember that it was very hot, there were many families and children visiting, and the visit coincided with my son completing a dinosaur project at the end of primary school. This would allow me to infer that it must have been in the summer holidays, specifically last August. In contrast to location-based theories, distance-based theories posit that the timing of an event is determined by its distance from the present. Thus, the date of an event may be inferred from a decline in vividness or accessibility of a memory. According to this view, if a memory is very vivid then it is more likely to be memory of a recent event, whereas if a memory is vague, then it is more likely to be a

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memory of an older event. Phrased in this way, vividness of the event could relate to how much information about the event is available to recall, how strongly familiar the event feels, or both. Friedman argues that distance-based processes play a role in temporal memory in young children and in adults, required to make speeded responses (Friedman, 2001). It has also been suggested that distance-based processes may be relied upon more by older people (Bastin & Van der Linden, 2005). It is possible therefore that both location-based and distance-based processes contribute to memory for temporal order information. Friedman makes this argument, and further suggests that the two types of process have separate neurological bases. Both types of process are likely to involve mnemonic circuits within the medial temporal lobe (MTL) region. But in addition, Friedman suggests that location-based processes involve the PFC (Curran & Friedman, 2003), whereas distancebased processes do not. According to this proposal, location-based processes may depend upon strategic aspects of encoding and retrieval, and should be reflected not only in a correlation between temporal order memory and associative memory, but also in a correlation between temporal order memory and performance on tests of executive function. In contrast, distance-based processes relying upon associative mechanisms within the hippocampus should simply be reflected in a correlation between temporal order memory and performance on tests of associative memory. Alternatively, distancebased processes relying upon familiarity may be reflected in a correlation between temporal order memory and performance on tests of item recognition. Recent neuroimaging studies have provided evidence consistent with the view that different types of temporal memory have different underlying neural substrates (Jenkins & Ranganath, 2010; St. Jacques, Rubin, LaBar, & Cabeza, 2008; Suzuki et al., 2002). Jenkins and Ranganath (2010) examined the relationship between neural activity at encoding and subsequent memory for temporal context. Memory for temporal context was assessed on two scales: coarse (i.e., the ability to indicate when, during the experiment, a specific stimulus appeared) and fine (i.e., the ability to recall the relative order of three stimuli presented in a given trial). They found a relationship between fine temporal accuracy and activity within the parahippocampal cortex. In contrast, they found a relationship between coarse temporal accuracy and activity in the right hippocampus and left PFC. There is evidence, therefore, that more than one type of process may be active in carrying out judgments of temporal order, and that these separate processes have different underlying neural substrates. If amnesic patients with discrepant, albeit overlapping, neuropathology rely differentially on these two kinds of process, this may explain a group difference which is sometimes observed between patients with MTL and diencephalic pathology. A group difference may be observed, for example, if neuropathology in one of the groups compromises to a greater extent brain regions underlying executive functioning which is proposed to underlie location-based processes. Conversely, a group difference may be observed if neuropathology in one of the groups compromises to a greater extent brain regions underlying associative memory, or familiarity, which is proposed to underlie distance-based processes. Two studies have shown that patients with diencephalic lesions are impaired relative to patients with MTL lesions on measures of temporal order memory (Hunkin & Parkin, 1993; Hunkin et al., 1994). However, other studies have failed to find a significant difference between patients with these two types of pathology (e.g., Downes et al., 2002; Kopelman et al., 1997). It is possible that different measures of temporal order memory place differential emphasis on separate underlying memory processes, and that the extent to which these processes are

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intact and functional determines whether or not any dissociation is observed between patients with discrepant neuropathology. The aim of this study is to examine memory performance in patients with MTL and diencephalic pathology on tests of between-list and within-list temporal memory, and to determine whether the observation of any group difference can be accounted for by the way in which memory for temporal order memory is assessed. It is proposed that different types of temporal order memory rely differentially on location-based and distance-based processes and these, in turn, may depend differentially on frontal or hippocampal mechanisms. Between-list and within-list temporal memory performance will thus be related to measures of executive function, associative memory and recognition memory to elucidate the processes underlying temporal order memory in patients with MTL and diencephalic amnesia.

EXPERIMENT 1: BETWEEN-LIST DISCRIMINATION Methods Participants Twelve patients with documented evidence of organic amnesia participated in the study. Five patients had presumed or confirmed damage to the MTL; seven patients had presumed damage to midline diencephalic structures following a medical diagnosis of WKS associated with prolonged alcoholism. All seven patients had a stable memory impairment and were abstinent from alcohol. Of the five patients with presumed or confirmed MTL damage, three (RB, CF, RS) had received a diagnosis of herpes simplex encephalitis, one (NM) had suffered from meningitis and one (CW) had suffered haemorrhage following rupture of a posterior cerebral artery aneurysm. Neuroimaging data were available for four of these patients and are summarized in the Appendix. Current general cognitive functioning was assessed using the Wechsler Adult Intelligence Scale - Revised (WAIS-R; Wechsler, 1981), and an estimate of pre-morbid functioning was given by the National Adult Reading Test (NART; Nelson, 1991). There was no significant difference between the two patient groups in terms of age, current IQ or estimated pre-morbid IQ (all ps > .5). Thus, one control group was constructed. This control group comprised 10 healthy volunteers matched to the patients in terms of age, WAIS-R FSIQ and NART FSIQ (all ps > .3). Mean age, and current and pre-morbid IQ for the three groups are shown in Table 1. Memory impairment in the patients was assessed using the Wechsler Memory Scale Revised (WMS-R; Wechsler, 1987), the Warrington Recognition Memory Test (WRMT; Warrington, 1984) and the Doors and People Test (D&P; Baddeley, Emslie, & NimmoTable 1. Age, current, and pre-morbid IQ in the three groups MTL

Age NART WAIS-R FSIQ

Diencephalic

Controls

Mean

SD

Mean

SD

Mean

SD

49.00 105.80 99.20

9.49 14.96 14.55

50.29 101.86 98.14

7.39 10.22 11.84

55.10 107.60 99.20

6.56 12.06 9.30

F = 1.423, p = .2655 F = 0.460, p = .6381 F = 0.021, p = .9797

Note. NART: National Adult Reading Test; Nelson (1991). WAIS-R FSIQ: Wechsler Adult Intelligence Scale – Revised, Full scale IQ; Wechsler (1981).

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Smith, 1994). Frontal lobe dysfunction was assessed using the modified Wisconsin Card Sorting Test (WCST; Nelson, 1976), Word Fluency (FAS; Benton, Hamsher, Varney, & Spreen, 1983), the Cognitive Estimation Test (CET; Shallice & Evans, 1978) and the Hayling and Brixton Tests (Burgess & Shallice, 1997). The results of these tests can be seen in Table 2. The two patient groups did not differ significantly on any measure. Although the group difference in number of perseverative errors on the WCST approached significance (F = 4.717, p = .0579), this result should be viewed with caution as the range of scores across all the patients was very small; patients made a maximum of two perseverative errors. We can therefore, assume that there was no significant difference between the two groups on this measure. Both patient groups showed a significant memory impairment scoring 1–2 SDs below the population mean on WMS-R tests of verbal and visual immediate memory and at least 2 SDs below the population mean on WMS-R delayed recall. Performance on the D&P and WRMT indicated that this memory impairment included both recall and recognition. In contrast, mean performance in both groups on the attention component of the WMS-R was average, and performance on the WCST was just below average; mean number of categories attained was at the 40–45th percentile (Obonsawin et al., 1999). A greater impairment was seen on FAS word fluency; FAS mean performance was approximately 1 SD below the mean of a group of age-appropriate normal individuals (Tombaugh, Kozak, Table 2. Performance on tests of memory and frontal dysfunction in the two patient groups MTL

WMS-general WMS-verbal WMS-visual WMS-delay WMS-attention D&P people D&P names D&P shapes D&P doors WRMT words WRMT faces WCST categories WCST perseverative errors FAS CET Hayling Brixton

Diencephalic

Mean

SD

Mean

SD

76.20 79.20 80.60 64.60 99.00 4.80 5.40 4.20 3.60 5.60 4.80 5.20 1.60 32.60 6.80 4.00 3.60

8.93 9.60 17.50 18.05 19.55 3.03 3.05 4.66 2.30 3.72 0.84 0.84 0.55 16.77 4.32 2.45 3.58

84.00 82.43 84.33 60.33 95.14 3.00 6.57 4.17 3.71 6.00 6.14 5.30 0.67 36.83 6.00 4.80 6.40

4.94 9.88 10.65 1.366 13.92 1.00 3.31 4.07 2.43 3.79 3.671 1.21 0.82 11.22 4.73 3.27 1.14

F F F F F F F F F F F F F F F F F

= = = = = = = = = = = = = = = = =

3.388, p 0.319, p 0.191, p 0.340, p 0.161, p 2.208, p 0.389, p 0.001, p 0.007, p 0.033, p 0.629, p 0.043, p 4.720, p 0.250, p 0.840, p 0.192, p 2.780, p

= = = = = = = = = = = = = = = = =

.0988 .5849 .6725 .5739 .6964 .1681 .5468 .9902 .9362 .8603 .4462 .8402 .0579 .6285 .7784 .6732 .1340

Note. WMS-R: Wechsler Memory Scale (indexes); Wechsler (1987); [Population mean 100, SD 15]. WRMT: Warrington Recognition Memory Test (scaled scores); Warrington (1984); [Population mean 10, SD 3]. D&P: Doors and People Test (scaled scores); Baddeley et al. (1994); [Population mean 10, SD 3]. WCST: Wisconsin Card Sorting Test (raw scores); Nelson (1976); [Population norm 50th percentile 6 categories; 5.2 and 5.3 categories 40-45th percentile (Obonsawin et al., 1999)]. FAS: FAS Word Fluency Test (raw scores); Benton et al. (1983); [Population mean 44.7, SD 11.2 (Tombaugh et al., 1999)]. CET: Cognitive Estimation Test (raw scores); Shallice and Evans (1978); Hayling, Brixton: The Hayling and Brixton Tests; Burgess and Shallice (1997); [Abnormal cut-off ≤2].

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& Rees, 1999) and comparable to the mean of a group of patients with frontal lobe lesions (MacPherson et al., 2008). High scores on the CET reflect frontal impairment; the group means in the current study are comparable with those reported by Kopelman et al. (1997) in their patients with diencephalic and temporal lobe amnesia, and reflect moderate impairment. In the Hayling and Brixton tests, all group means were above the cut-off for abnormal performance but tended to lie in the poor to low average range (MTL group) or the low average to average range (diencephalic group). In summary, both patient groups showed a significant memory impairment accompanied by mild to moderate frontal dysfunction, but none of the tests allowed a dissociation to be made between the two patient groups. The study was approved by the local NHS Research Ethics Committee. All participants gave informed consent to participate.

Materials The stimuli were 96 words selected from the Psycholinguistic Database (Quinlan, 1992). These words were used to create two between-list recognition tests: one to be run under incidental study conditions, and one to be run under intentional study conditions. Low frequency words were chosen as we wished to enhance participants’ recognition of the stimuli, and previous work has indicated that low frequency words are more easily recognized. The words were divided into 8 sets of 12 that were matched in terms of frequency, imageability, familiarity and concreteness. Two sets were designated as targets for the incidental condition, and two sets were designated as targets for the intentional condition; two sets were designated as distractors for the incidental condition, and two sets were designated as distractors for the intentional condition. The materials were counterbalanced so that those lists that served in the incidental condition for half the participants served in the intentional condition for the remainder of the participants.

Procedure The experiment was presented on computer (Apple Macintosh Powerbook 540c), with all study and test stimuli presented in upper case ‘Times’ font, size 24 point. At study, participants were presented with two lists of words. Each list comprised 12 words, and the words were presented one at a time at the centre of the screen. In order to equate recognition performance in the patients and controls, study exposure duration was varied across participants. All control participants were given a 4 s study exposure duration, whereas most (10/12) patients were given a 7 s study exposure duration. For the remaining two patients (one MTL, one diencephalic), there was independent evidence that item recognition was good (WRMT), and these two patients were therefore given a study exposure duration of 4 s. For all participants, the inter-stimulus interval (ISI) was 1 s. Presentation of the two lists was separated by a delay of 15 min during which participants carried out a non-verbal task. There was a further conversation-filled delay of 2 min after presentation of the second list before memory testing began. The experiment was run under both incidental and intentional study conditions, so that each subject was run twice, first with incidental instructions and second with intentional instructions. The delay between incidental and intentional conditions was 1 week. At study, in the incidental condition, participants were instructed to look at each word as it appeared on the screen and to make a judgment as to whether the object represented by that word was ‘man-made’ (e.g., BRACELET) or ‘natural’ (e.g.,

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EARTHWORM). Participants were not informed that their memory would subsequently be tested. At study, in the intentional condition, participants were told that they would see two lists of words, and that the two lists would be separated by a 15-minute delay. They were told that they should try and remember both the words themselves and in which list each word appeared. Participants were informed that their memory for the words and list membership would be tested later. In order to be consistent with the incidental condition, participants were also asked to make the ‘man-made’/’natural’ decision for each item. Testing was carried out after a conversation-filled delay of 2 min. Participants were given a two-alternative forced choice test. Each of the studied words (targets) was paired with a distractor of similar word-length. The target and its distractor were displayed horizontally on the screen. The target-distractor pairs were the same for all participants, but the pairs were presented in random order for each subject. Half the targets were displayed on the left side of the screen and half on the right. Participants were required to indicate which of the two words they had seen before (recognition), and in which list the word had appeared (between-list discrimination). All responses were made verbally, and were recorded by the experimenter.

Results Between-list discrimination performance was based on items that were correctly recognized, that is, discrimination performance was contingent upon correct recognition. One of the MTL patients showed very poor recognition in one of the conditions (NM 54%). His data were therefore removed from the analysis. Minimum recognition performance in the remainder of the participants was 66%. Since recognition performance (and therefore the number of opportunities for discrimination) varied across participants, discrimination scores were converted to z-scores using a correction based on the binomial distribution (see Hunkin et al., 1994). This is a more appropriate way of representing discrimination performance contingent upon correct recognition because it compensates for variations in level of recognition performance. For consistency and ease of analysis, the recognition scores were also converted to z-scores, using the same formula. The data are summarized in Figure 1. The data were analysed in a three-way ANOVA with group (MTL, diencephalic, control) as a between-subjects factor, and encoding condition (incidental, intentional) and task (recognition, discrimination) as within-subjects factors. There was a significant main effect of group (F(2,18) = 13.234, p = .0003). Post-hoc Newman-Keuls analysis indicated that both patient groups were impaired relative to the control group (p < .05), but the difference between the two patient groups did not reach significance. There was a significant main effect of task (F(1,18) = 150.641, p = .0001) reflecting better performance on the recognition task than the discrimination task. There was also a significant task 9 group interaction (F(2,18) = 15.537, p = .0001). There was no significant effect of encoding condition (p > .8), nor any other interaction (ps > .18). The significant task 9 group interaction was explored by two-way ANOVAs (group as a betweensubjects factor, encoding condition as a within-subjects factor) on the recognition and discrimination data separately. For the recognition data, there were no main effects or interaction (all ps > .2). Specifically, there was no significant effect of group, indicating that the manipulation of study time was successful in equating levels of recognition in the three groups. For the discrimination data, however, there was a significant main effect of group (F(2,18) = 23.565, p = .0001). Newman-Keuls analysis indicated that both patient groups were impaired relative to the control group and that, in addition, the diencephalic

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z-score/units of standard deviation

4 3.5 3 2.5 2 1.5 1 0.5 0 Recog

Discrim MTL

Recog

Discrim

Recog

Diencephalic

Discrim

Control

Figure 1. Experiment 1: Recognition and between-list discrimination performance as a function of group (error bars = SE).

group was significantly impaired relative to the MTL group (p < .05). There was no effect of encoding condition (p > .5) nor a group 9 encoding condition interaction (p > .3). To examine whether discrimination performance can be accounted for by extent of memory impairment or frontal lobe dysfunction, a correlational analysis was carried out. To maximize the stability of the data and to reduce the number of correlation coefficients calculated, the scores in the incidental and intentional conditions were averaged. This mean discrimination score was correlated with a composite verbal recall factor, a composite verbal recognition factor and a composite frontal factor. Each of these factors was the mean z-score (calculated from the individual scores within the patient sample) for verbal recall (D&P people, WMS-verbal), verbal recognition (D&P names, WRMT words) and frontal (FAS, CET, Hayling, Brixton) tests. (WCST scores did not contribute to the composite frontal factor because of the limited range in performance across patients.) This analysis indicated a significant correlation between discrimination performance and verbal recognition (r(9) = 0.564, p = 0.0354; one-tailed) but the remaining correlations were not significant (both ps > .15).

EXPERIMENT 2: WITHIN-LIST DISCRIMINATION Methods Participants The participants were five patients with MTL damage, four patients with diencephalic damage, and 10 healthy control participants reported in Experiment 1. Three of the diencephalic patients reported in Experiment 1 (GL, MD, JO) were not available for this experiment.

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Materials A total of 352 low frequency words were selected from the Oxford Psycholinguistic database (Quinlan, 1992). These words were used to create a series of two-alternative recognition tests and two-alternative within-list discrimination, or recency, tests. The 352 words were divided into five sets: Set, 1 n = 72; Set 2, n = 72, Set 3, n = 64; Set 4, n = 64; Set 5, n = 80. The five sets were matched in terms of word frequency, concreteness, and number of letters (all ps > .48). Set 1 comprised words used as the first member of a pair in the recency judgment. Set 2 comprised words used as the second member of a pair in the recency judgment. Set 3 comprised the target words in the recognition trials. Set 4 comprised the words used as distractors in the recognition trials. Finally, Set 5 comprised ‘filler’ words used to increase the number of trials so that the requisite number of intervals and ratios could be achieved.

Design Recognition was tested at eight different study-test lags (2, 4, 8, 12, 16, 32, 64, 128). For example, in the sequence ‘poison . . . exterior . . . measles/poison . . . hay . . . quarter . . . exterior/trumpet’, the word ‘poison’ is tested at a study-test lag of 2, whereas the word ‘exterior’ is tested at a study-test lag of 4. There were eight trials at each lag. Within-list discrimination, or recency, was tested at nine different ‘interval-pairs’. Each interval-pair is defined by the respective study-test lags of the two items being compared; for example, in the sequence ‘hut . . . pendulum . . . boundary . . . trolley . . . hut/boundary’, the pair ‘hut/boundary’ corresponds to an interval-pair of 2/4 (see Figure 2). The nine interval-pairs used were: 2/4, 2/16, 2/32, 4/8, 4/32, 4/64, 8/16, 8/64, and 8/128. There were eight trials at each interval-pair. The use of these nine interval-pairs allowed us to investigate the effects of manipulating two variables: (1) study-test lag and (2) lag ratio.

Study-test lag This is the distance between study and test of the most recently studied item within a test pair. By collapsing across the ratio of the respective lags of the two items in an intervalpair, it is possible to investigate the effect of an increase in study-test lag, that is, increasing the distance between the most recent of the two items and test. There are three levels of study-test lag: 2 (2/4, 2/16, 2/32), 4 (4/8, 4/32, 4/64), and 8 (8/16, 8/64, 8/128). Lag ratio This is the ratio of the distance between study and test of the two items in a test pair. By collapsing across study-test lag, it is possible to investigate the effect of an increase in lag ratio, that is, increasing the ratio of the distances between the two items being tested. There are three levels of lag ratio: 1:2 (2/4, 4/8, 8/16), 1:8 (2/16, 4/32, 8/64), and 1:16 (2/ 32, 4/64, 8/128). Manipulation of these two variables enabled us to investigate the effect of proximity of the items in the study list (lag ratio) as well as the effect of time between study and test (study-test lag). Specifically, it was of interest whether one or both patient groups showed a differential impairment in ability to make recency judgments when these judgments were made between items close together in the study list (i.e., small lag ratio) and whether there was any relative advantage for items that had been studied very recently (i.e., short study-test lag).

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Lag = 4 Study

Study Recency test Study

web trolley

flute

poison

hut boundary

Time Study

Study Study

pendulum

trolley

boundary

Interval-pair = 2/4

hut

Figure 2. Schematic to illustrate sequence of events in within-list discrimination task (Experiment 2). On recognition test trials, each pair of words was accompanied by the question: ‘Which of these words did you see BEFORE?’. On recency test trials, each pair of words was accompanied by the question: ‘Which of these words did you see MORE RECENTLY?’.

Procedure The study comprised a pseudorandom intermixed sequence of study (n = 288) and test (n = 136) trials. Participants were told that they would see a series of words presented one at a time on the computer screen. They were asked to read each word aloud, and to try to remember the words in their order of appearance. At intervals throughout the study, participants were presented with two words presented simultaneously. These two words were accompanied by a question at the bottom of the screen: ‘Which of these words did you see BEFORE?’ (recognition test) or ‘Which of these words did you see MORE RECENTLY?’ (within-list or recency judgment). If participants were unsure, they were asked to guess. Study items were presented for 1 s, with an ISI of 1 s. Test items were selfpaced, although participants were encouraged to respond fairly quickly. Participants were given a practice sequence and the opportunity to ask questions before the proper sequence began.

Results For both recognition and within-list discrimination data, the proportion identified correctly at each study-test lag was calculated. The recognition data, which are summarized in Figure 3, were analysed in a two-way ANOVA with group (MTL, diencephalic, control) as a between-subjects factor and lag (2, 4, 8, 12, 16, 32, 64, 128)

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MTL Diencephalic Control

Percentage correct

100

80

60

40

20

2

4

8

12 16 Lag

32

64

128

Figure 3. Recognition performance as a function of lag (error bars = SE).

as a within-subjects factor. There were significant main effects of group (F (2,16) = 12.843, p = .0005) and lag (F(7,112) = 13.355, p = .0001), the latter reflecting poorer performance with increasing lag, but no interaction (p > .4). Newman-Keuls analysis indicated that each patient group was impaired relative to the controls (p < .05), but the two patient groups did not differ. In order to determine whether or not recognition performance at each lag was above chance, individual t-tests for each group were carried out. This information is of value when considering subsequent within-list discrimination performance. These analyses indicated that recognition performance in all three groups was above chance for lags 2, 4, and 8 (ps < .05). Thereafter, recognition performance in the MTL group at lags 12, 32, 64, and 128 and in the diencephalic group at lags 16, 64 and, 128 was not significantly above chance. The within-list discrimination (or recency) data are summarized in Figures 4 and 5. The data from the nine conditions designed to examine the effects of lag ratio and studytest lag were analysed in a three-way ANOVA with group (MTL, diencephalic, control) as a between-subjects factor, and lag ratio (1:2, 1:8, 1:16) and study-test lag (of more recent item; 2, 4, 8) as within-subjects factors. There was a significant main effect of group (F (2,16) = 53.879, p = .0001). Newman-Keuls analysis indicated that each patient group was impaired relative to the controls and that, in addition, the diencephalic group was significantly impaired relative to the MTL group (p < .05). There were also significant main effects of lag ratio (F(2,32) = 8.570, p = .001) and study-test lag (F(2,32) = 12.268, p = .0001). Pairwise t-tests indicated that performance in the 1:2 lag ratio was significantly lower than that in the 1:8 lag ratio (t(18) = 4.93, p = .0001), but the other pairwise comparisons failed to reach significance (1:2 vs. 1:16: t(18) = 2.00, p = .0605; 1:8 vs. 1:16: t(18) = 1.84, p = .0823). Further pairwise t-tests indicated that when collapsed across lag ratio, a study-test lag of 2 was associated with significantly better performance than study-test lags of both 4 and 8 (2 vs. 4: t(18) 2.74, p = .0134; 2 vs. 8: t(18) = 4.90,

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Percentage correct

100 80 60 40 MTL

20

Diencephalic Control

0

2

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Figure 4. Within-list discrimination performance as a function of study-test lag (error bars = SE). 120

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Figure 5. Within-list discrimination performance as a function of lag ratio (error bars = SE).

p = .0001), but performance at the study-test lags of 4 and 8 did not differ significantly (t (18) = .94, p = .36). In addition to the significant main effects of lag ratio and study-test lag, each of these factors showed a significant interaction with group (lag ratio 9 group: F (4,32) = 3.569, p = .0162; study-test lag 9 group: F(4,32)3.358, p = .0210), and there was a three-way lag ratio 9 study-test lag 9 group interaction (F(8,64) = 2.802, p = .01). To examine whether the three groups responded differently to the manipulation of study-test lag and lag ratio, the interactions were explored by separate two-way ANOVAs for each condition (study-test lag, lag ratio).

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For study-test lag, there was a significant main effect of group (F(2,16) = 41.308, p = .0001). Neuman-Keuls post-hoc analysis indicated that, as in the omnibus analysis, each patient group was impaired relative to the controls and that, in addition, the diencephalic group was significantly impaired relative to the MTL group (ps < .05). There was also a significant main effect of study-test lag (F(2,32) = 9.326, p = .0006), reflecting poorer performance with increased distance between study and test, and there was a significant group 9 study-test lag interaction (F(4,32) = 3.375, p = .0206). To interpret this interaction and to look for any group differences, separate one-way ANOVAs were conducted at each level of the independent variable. At a study-test lag of 2, there was a significant main effect of group (F(2,16) = 5.679, p = .0137); post-hoc analysis indicated a significant difference between the diencephalic group and both the control group and the MTL group (p < .05), but there was no significant difference between the MTL group and the control group. At a study-test lag of 4, there was also a significant main effect of group (F(2,16) = 26.988, p = .0001). Post-hoc analysis indicated a significant difference between each patient group and the controls (p < .05) but not between the two patient groups. Similarly, at a study-test lag of 8, there was a significant main effect of group (F (2,16) = 14.568, p = .0002) with post-hoc analysis indicating a significant difference between each patient group and the controls (p < .05) but not between the two patient groups. For lag ratio, there was a significant main effect of group (F(2,16) = 53.879, p = .0001). Neuman-Keuls post-hoc analysis indicated that, as in the omnibus analysis and the study-test lag analysis, each patient group was impaired relative to the controls and that, in addition, the diencephalic group was significantly impaired relative to the MTL group (p < .05). There was also a significant main effect of lag ratio (F(2,32) = 8.570, p = .0010) reflecting better performance with a larger lag ratio, and there was a significant group 9 lag ratio interaction (F(4,32) = 3.569, p = .0162). To interpret this interaction and to look for any group differences, separate one-way ANOVAs were conducted at each level of the independent variable. At a lag ratio of 1:2, there was a significant main effect of group (F(2.16) = 10.033, p = .0015). Post-hoc analysis indicated a significant difference between the diencephalic group and both the control group and the MTL group (ps < .05), but there was no significant difference between the MTL group and the control group. At a lag ratio of 1:8, there was also a significant main effect of group (F (2,16) = 20.692, p = .0001). Post-hoc analysis indicated a significant difference between each patient group and the controls (p < .05) but not between the two patient groups. Similarly, at a lag ratio of 1:16, there was a significant main effect of group (F (2,16) = 27.390, p = .0001) with post-hoc analysis indicating a significant difference between each of the patient groups and the controls (p < .05) but not between the two patient groups. To summarize, the diencephalic group was impaired relative to the control group and the MTL group on within-list discrimination performance when recency judgments were made at the shortest study-test lag (two items) and the smallest lag ratio (1:2). Under these conditions, the MTL group performed similarly to the controls. However, at all other study-test lags and lag ratios both diencephalic and MTL groups were impaired relative to the controls, and there was no significant difference between the two patient groups. To examine whether within-list discrimination performance can be accounted for by extent of memory impairment or frontal lobe dysfunction, a correlational analysis was carried out. Mean recency performance (averaged across all study-test lags and lag ratios) was correlated with the recall, recognition, and frontal composite factors indicated in Experiment 1. There were no significant correlations (all ps > .25).

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GENERAL DISCUSSION In Experiment 1, ‘Between-list Discrimination’, the three groups (MTL, diencephalic, controls) were well matched on recognition but differed significantly on discrimination. Specifically, the two patient groups were not only impaired relative to the controls but, in addition, the diencephalic group was impaired relative to the MTL group. A correlational analysis indicated a significant correlation between discrimination performance and a composite recognition memory measure. In Experiment 2, ‘Within-list Discrimination’, both patient groups were impaired relative to the controls on the measure of recognition, but the two patient groups did not differ significantly from each other. In terms of the ability to make within-list discriminations, or recency judgments, the two patient groups were impaired relative to the controls. Moreover, the diencephalic group was significantly impaired relative to the MTL group on this measure. There were no significant correlations between recency judgment and any one of the composite memory or frontal lobe measures. More detailed analysis of the data from Experiment 2 revealed that the difference between the two patient groups on the within-list discrimination measure was only significant at the shortest study-test lag (two items) and the smallest lag ratio (1:2). Under these conditions, the MTL group did not perform significantly differently from the control group. For the remaining study-test lags and lag ratios, both patient groups were impaired relative to the controls and there was no significant difference between them. It is unlikely that the difference between the two patient groups on within-list discrimination can be accounted for by poor recognition performance. First, the diencephalic group was impaired relative to the MTL group despite comparable recognition performance. Second, recognition performance in the diencephalic group was significantly above chance for lags up to and including 12. This allowed an examination of within-list discrimination in the context of relatively good recognition performance. The study-test lags used in the within-list discrimination task ranged from 2 to 8. Thus, at all study-test lags, at least one member of the test pair would have been within the range at which recognition performance was above chance for all groups. Despite this, within-list discrimination performance in the diencephalic group was impaired at the shortest study-test lag (two items). Poor discrimination performance cannot thus be attributed to poor recognition performance, but is consistent with specific difficulties in making the temporal order judgment. It appears that, at the shortest studytest lag and the smallest lag ratio, MTL patients were able to make the temporal order judgment with similar accuracy to the controls, but with longer lags and larger lag ratios, these patients also showed impairment. It is also unlikely that the relative impairment of the diencephalic group at the shortest study-test lag (two items) and smallest lag ratio (1:2) could be accounted for by an additional working memory impairment. First, there was no evidence that the diencephalic patients were more impaired on working memory tasks (e.g., WMS-R attention) and, second, the lag ratio of 1:2 included individual recency judgments which would be considered to lie outside the scope of working memory (e.g., 4 vs. 8, 8 vs. 16). Furthermore, an MTL-diencephalic group difference had also been demonstrated in between-list discrimination, a task that could not be considered to tap working memory. To summarize, the diencephalic group was impaired relative to the MTL group on two measures of temporal order memory. This relative impairment in the diencephalic group cannot be accounted for by an impairment in item recognition or working memory, nor

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can it be accounted for by the way in which temporal order memory was assessed, as the impairment was observed for both between-list and within-list temporal order judgments. The overall results are consistent with a number of studies that have demonstrated a significant difference between MTL and diencephalic patients in terms of their ability to make temporal order judgments (Hunkin & Parkin, 1993; Hunkin et al., 1994; Shimamura et al., 1990). Several studies, however, have failed to identify a difference between MTL and diencephalic patients. Using a list discrimination procedure similar to that used in Experiment 1, Downes et al. (2002) found no significant difference between patients whose amnesia resulted from Korsakoff’s syndrome and those whose amnesia resulted from MTL damage. However, as the authors point out, both patient groups scored at chance on the list discrimination measure, so a floor effect on temporal order memory made it impossible to determine whether one group was impaired relative to the other. In a further list discrimination procedure, Kopelman et al. (1997) found no difference between patients with diencephalic and MTL pathology, but noted that only the diencephalic group was impaired relative to the controls. In this study, the diencephalic group was impaired relative to the MTL group on both temporal order memory tasks yet it performed similarly to the MTL group on standardized measures of both memory and frontal lobe dysfunction. One possible explanation for this pattern of results is that the temporal order memory tasks provide a more sensitive measure of cognitive dysfunction. Thus, a group difference emerges only on the temporal order memory tasks because they are more difficult. This is a feasible explanation given recent neuroimaging evidence that extent of hippocampal activation during encoding was related to amount of information subsequently available at retrieval (Qin, van Marle, Hermans, & Fernandez, 2011). One could argue that, to make accurate temporal order judgments, access to increased amounts of contextual information is required. Amnesic patients, in whom the hippocampal system is compromised, will therefore have greater difficulty retrieving temporal contextual information than less extensive associative information typically tapped in standardized memory tests. Thus, temporal order memory tasks will be more sensitive to a deficit in associative memory than the standardized memory tasks. An alternative explanation is that temporal order memory is dependent upon both mnemonic processes and executive function but that the type of executive function that underlies temporal order memory is different from the type of executive function that is tapped by the tests used in this study (FAS word fluency, CET, Hayling & Brixton). In other words, it is suggested that there may be other kinds of executive function that are not tapped by tests in this study but which are particularly important for temporal order memory, and which may be affected differentially in the two patient groups. This seems very plausible given that Korsakoff patients are known to have extensive frontal lobe dysfunction (Brokate et al., 2003; Oscar-Berman, 2012), in contrast to the more subtle effects mediated by the dysfunctional thalamic-frontal connections that probably exist in most MTL patients (Mayes et al., 2001; Shoqeirat, Mayes, MacDonald, Meudell, & Pickering, 1990). As indicated in the Appendix, neuroimaging data were not available for the current Korsakoff patients; frontal lobe pathology is, therefore, presumed rather than verified. Nevertheless, there is strong evidence from the literature that WKS is associated with PFC pathology (Jung, Chanraud, & Sullivan, 2012; Kril, Halliday, Svoboda, & Cartwright, 1997), which is reflected in poor performance on tests of frontal lobe dysfunction (Oscar-Berman, 2012). Furthermore, apathy is a frequent feature of frontal lobe dysfunction in Korsakoff patients (Oscar-Berman, 2012; Victor, Adams, & Collins, 1989). This is likely to reduce participants’ motivation and increase the likelihood that

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responses would be made using familiarity or distance-based judgments rather than invoke more effortful location-based processes. Typically, MTL patients are not apathetic, and we can speculate that the superior performance of the MTL patients in Experiment 1, and on the shortest study-test lag and smallest lag ratio in Experiment 2, may reflect some use of residual frontally mediated location-based processes. According to this view, it should be possible to administer a wide range of theoretically motivated tests of frontal function, such that an impairment on one or more of these tests predicts patients’ relative impairment on tests of temporal order memory. In terms of which type of theory (location-based or distance-based) best accounts for temporal order memory, the results of the present study are consistent with responses being based on distance-based processes in the current patient cohort. The significant correlation between between-list discrimination and recognition memory can be interpreted to reflect a reliance on familiarity in making between-list judgments. Although familiarity-based recognition is not thought to be normal in global amnesic patients (Yonelinas, Kroll, Dobbins, Lazzara, & Knight, 1998), it may still be less impaired than recall, and therefore may be used as the basis for patients’ temporal order judgments. In the between-list discrimination task of Experiment 1, there are likely to be larger familiarity differences between items appearing in two different lists, compared with items appearing in the same list in Experiment 2 (within-list discrimination). This would account for the significant correlation between temporal order memory and recognition memory observed in Experiment 1 that was absent in Experiment 2. In contrast to the amnesic patients, there is evidence that normal control subjects invoke location-based processes to make temporal order judgments (Bastin, Van der Linden, Michel, & Friedman, 2004; Curran & Friedman, 2003). The use of location-based processes, involving both mnemonic and executive functions, is likely to provide much greater accuracy of responding in normal individuals. Evidence suggests that when responses are based on familiarity, even when familiarity-based recognition is intact, temporal order memory can be poor (Mayes et al., 2001).

Conclusion In this study, amnesic patients with diencephalic pathology were impaired relative to those with MTL pathology on two tests of temporal order memory, despite the two patient groups performing similarly on standardized tests of memory and executive function. Contrary to our hypothesis, the MTL-diencephalic group difference could not be accounted for by the way in which memory for temporal context was assessed, as the group difference was apparent on both within-list and between-list tasks. The results are consistent with patients’ temporal order memory responses (at least for between-list discrimination) being based on familiarity, that is, distance-based processes. In contrast, reconstructive location-based processes mediated by the PFC (Curran & Friedman, 2003) may underlie healthy participants’ performance on between-list discrimination (Parkin, Walter, & Hunkin, 1995). It is parsimonious to argue that associative memory impairment and/or frontal dysfunction in the amnesic patients results in a shift to a reliance upon familiarity or distance-based processes. Future work on a larger sample of patients, using a wider range of tests of executive function, including those sensitive to apathy, should allow us to test this hypothesis and to determine whether, under conditions in which amnesic patients perform similarly to controls (e.g., MTL patients at the shortest study-test lag in Experiment 2), patients invoke residual frontally-mediated processes to aid their performance.

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Acknowledgement Thanks to Jim Stone for statistical advice and helpful discussions.

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Appendix Neuroimaging data on individual patients Neuroimaging data were available for four of the 12 patients (RS, CF, CW, NM), and their neuropathology has already been described elsewhere (Holdstock, Gutnikov, Gaffan, & Mayes, 2000). MRI indicated that Patient RS had a bilateral hippocampal lesion that extended into the posterior portion of the amygdala, although the volume of the amygdala was within the normal range. RS’s hippocampus was small throughout its length bilaterally with greater volume loss at the head. The left parahippocampal, entorhinal and perirhinal cortices were partially damaged with also some damage to the perirhinal cortex on the right. The volumes of both temporal lobes were found to be significantly smaller than those of a group of age-matched control subjects. No other focal lesions were evident, although there was some general cortical atrophy and ventricular enlargement. Patient CF was found to have complete damage to the amygdala, hippocampus, parahippocampal cortex, perirhinal cortex and entorhinal cortex on the right with additional partial damage in this hemisphere to the superior and middle temporal gyri, the occipito-temporal gyrus and the insular cortex. CF also had some damage to the amygdala,

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and the parahippocampal, perirhinal and entorhinal cortices on the left. Patient CW had CT evidence consistent with damage caused by rupture of a posterior cerebral artery aneurysm. The CT scan showed damage to the posterior temporal region, a zone of reduced density in the occipital cortex and bilateral MTL damage that was more extensive on the right. MRI indicated that Patient NM had partial bilateral MTL damage to the amygdala and head, body and tail of the hippocampus, as well as the parahippocampal, entorhinal and perirhinal cortices. In addition, there was slight atrophy of the superior frontal and parietal lobes, mammillary bodies and cerebellum. No other focal lesions were evident. No MRI or CT data were available for any of the WKS patients. However, studies in which neuropathology associated with WKS has been investigated have indicated that this syndrome is characterized by midline damage to the diencephalon, including the dorsomedial thalamic nucleus and the mammillary bodies bilaterally (Victor et al., 1989). A more recent study comparing alcoholic patients with and without Korsakoff’s psychosis found that these two types of patient were differentiated by neuronal loss in the anterior thalamic nuclei in the Korsakoff patients (Harding, Halliday, Caine, & Kril, 2000). The effect of long-term alcohol consumption on the PFC is well established. There is evidence from both post-mortem studies (Kril et al., 1997) and in vivo neuroimaging studies (see Jung et al. (2012) for review) that long-term alcohol consumption is associated with PFC pathology, and this is the result of both a reduction in neuronal density and a reduction in white matter volume in the PFC (Kril et al., 1997). This pathology is reflected in poor performance on tests of frontal lobe dysfunction (Oscar-Berman, 2012). We can assume, therefore, that the WKS patients in the current study would have neuropathology that included both damage to subcortical structures critically related to memory function and damage to PFC that is likely to result in executive dysfunction. Of the four patients in the MTL group for whom scan data were available, none had any focal lesions in the PFC. Two patients had some general cortical atrophy (RS and NM) with that in NM involving the superior frontal cortex. Furthermore, given the reciprocal projections from MTL structures to PFC, it needs to be considered whether executive function in MTL patients may also be comprised, and whether these patients may also show impairment on tests sensitive to frontal lobe dysfunction.