Accelerated long-term forgetting in temporal lobe but not idiopathic generalised epilepsy.

Temporal lobe epilepsy (TLE) has been associated with the phenomenon of accelerated long-term forgetting (ALF), in which memories are retained normally over short delays but are then lost at an accelerated rate over days or weeks. The causes of ALF, and whether it represents a consolidation deficit distinct from the one associated with forgetting over short delays, remain unclear. In addition, methodological issues have made results of some previous studies difficult to interpret. This study used improved methodology to investigate the role of seizure activity in ALF. Forgetting was assessed in participants with TLE (who have involvement of temporal lobe structures) and idiopathic generalised epilepsy (IGE; in which seizures occur in the absence of identified structural pathology in the temporal lobes). Learning of novel stimuli was matched between patients with TLE, patients with IGE and healthy controls matched for age and IQ. Results indicated that the TLE group showed accelerated forgetting between 30-min and three-weeks, but not between 40-s and 30-min. In contrast, rates of forgetting did not differ between patients with IGE and controls. We conclude that (1) ALF can be demonstrated in TLE in the absence of methodological confounds; (2) ALF is unlikely to be related to the experience of epilepsy that does not involve the temporal lobes; (3) neither seizures during the three-week delay nor polytherapy was associated with ALF.

Change in background context disrupts performance on visual paired comparison following hippocampal damage.

The medial temporal lobe plays a critical role in recognition memory but, within the medial temporal lobe, the precise neural structures underlying recognition memory remain equivocal. In this study, visual paired comparison (VPC) was used to investigate recognition memory in a human patient (YR), who had a discrete lesion of the hippocampus, and a group of monkeys with neonatal hippocampal lesions, which included the dentate gyrus, and a portion of parahippocampal region. Participants were required to view a picture of an object on a coloured background. Immediately afterwards, this familiar object was shown again, this time paired with a novel object. All participants displayed a novelty preference, provided the background on which the objects were shown was the same as the one used during the learning phase. When the background of the familiar object was changed between initial familiarization and test, only the control subjects showed a novelty preference; the hippocampal-lesioned monkeys and patient YR showed null preference. The results are interpreted within Eichenbaum and Bunsey's [Eichenbaum, H., & Bunsey, M. (1995). On the binding of associations in memory: Clues from studies on the role of the hippocampal region in paired-associate learning. Current Directions in Psychological Science, 4, 19-23] proposal that the hippocampus facilitates the formation of a flexible representation of the elements that make up a stimulus whereas the parahippocampal region is involved in the formation of a fused representation.

Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition.

In this study, we have examined visual recognition memory in a patient, YR, with discrete hippocampal damage who has shown normal or nearly normal item recognition over a large number of tests. We directly compared her performance as measured using a visual paired comparison task (VPC) with her performance on delayed matching to sample (DMS) tasks. We also investigated the effect of retention interval between familiarisation and test. YR shows good visual recognition with the DMS task up to 10 s after the familiarisation period, but only shows recognition with the VPC task for the shortest retention interval (0 s). Our results are consistent with the view that hippocampal damage disrupts recollection and recall, but not item familiarity memory.

Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus.

There is disagreement about whether selective hippocampal lesions in humans cause clear item recognition as well as recall deficits. Whereas Reed and Squire (Behav Neurosci 1997;111:667-775) found that patients with adult-onset relatively selective hippocampal lesions showed clear item recognition deficits, Vargha-Khadem et al. (Science 1997;277: 376-380, Soc Neurosci Abstr 1998;24:1523) found that 3 patients who suffered selective hippocampal damage in early childhood showed clear recall deficits, but had relatively normal item recognition. Manns and Squire (Hippocampus 1999;9:495-499) argued, however, that item recognition may have been spared in these patients because the early onset of their pathology allowed compensatory mechanisms to develop. Therefore, to determine whether early lesion onset is critical for the relative sparing of item recognition and to determine whether its occurrence is influenced by task factors, we extensively examined item recognition in patient Y.R., who has pathology of adult-onset restricted to the hippocampus. Like the developmental cases, she showed clear free recall deficits on 34 tests, but her item recognition on 43 tests was relatively spared, and markedly less disrupted than her recall. Her item recognition performance relative to that of her controls was not significantly influenced by whether tests tapped visual or verbal materials, had a yes/no or forced-choice format, contained few or many items, had one or several foils per target item, used short or very long delays, or were difficult or easy for normal subjects. Interestingly, YR's bilateral hippocampal destruction was greater than at least 2 of the 3 patients of Manns and Squire (Hippocampus 1999;9:495-499). The possible reasons why item recognition differs across patients with relatively selective hippocampal damage of adult-onset and how the reasons that are truly critical can be best identified are discussed.

Temporal order memory in patients with Korsakoff's syndrome and medial temporal amnesia.

Two groups of patients with global amnesia resulting either from Korsakoff's syndrome (KS) or from medial temporal lobe (MTL) damage were compared with groups of matched healthy control subjects on a list discrimination paradigm. Item recognition memory was matched across the amnesic and control groups in order to determine whether KS, but not MTL amnesics are disproportionately impaired on list discrimination as predicted by Parkin's [Functional significance of etiological factors in human amnesia. In: Squire LR, Butters N, editors. Neuropsychology of memory, 2nd ed. New York: The Guilford Press, 1992] hypothesis. However, both patient groups were impaired disproportionately on the temporal order memory task, which is inconsistent with Parkin's hypothesis. It remains possible that the KS patients are more disproportionately impaired than those with MTL damage because both patient groups performed at floor on the list discrimination task. The results are consistent with theories that postulate a critical role for the hippocampus in the kind of associative memory which underlies memory for temporal order, but not in recognition of single items or arbitrary associations between items of similar kinds.

Predicting spontaneous recovery of memory.

Long after a new language has been learned and forgotten, relearning a few words seems to trigger the recall of other words. Neural-network models indicate that this form of spontaneous recovery may result from the storage of distributed representations, which are thought to mediate human memory. Here we use a psychomotor learning task to show that a corresponding effect of spontaneous memory recovery occurs in human subjects.

British memory research: a journey through the 20th century.

A century of research in memory has generated a wealth of knowledge encompassing theoretical developments within a number of distinct domains of memory. The aim of this article is to explore the progress made in memory research during the 20th century, to indicate critical influences on the direction of research, and to illustrate the important contribution made by British researchers. This article is confined to human memory research, and reviews research findings from the various psychological disciplines studied over the past 100 years.

When is now? Perception of simultaneity.

We address the following question: Is there a difference (D) between the amount of time for auditory and visual stimuli to be perceived? On each of 1000 trials, observers were presented with a light-sound pair, separated by a stimulus onset asynchrony (SOA) between -250 ms (sound first) and +250 ms. Observers indicated if the light-sound pair came on simultaneously by pressing one of two (yes or no) keys. The SOA most likely to yield affirmative responses was defined as the point of subjective simultaneity (PSS). PSS values were between -21 ms (i.e. sound 21 ms before light) and +150 ms. Evidence is presented that each PSS is observer specific. In a second experiment, each observer was tested using two observer-stimulus distances. The resultant PSS values are highly correlated (r = 0.954, p = 0.003), suggesting that each observer's PSS is stable. PSS values were significantly affected by observer-stimulus distance, suggesting that observers do not take account of changes in distance on the resultant difference in arrival times of light and sound. The difference RTd in simple reaction time to single visual and auditory stimuli was also estimated; no evidence that RTd is observer specific or stable was found. The implications of these findings for the perception of multisensory stimuli are discussed.

Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions.

One kind of between-list and two kinds of within-list temporal order memory were examined in a patient with selective bilateral hippocampal lesions. This damage disrupted memory for all three kinds of temporal order memory, but left item and word pair recognition relatively intact. These findings are inconsistent with claims that (1) hippocampal lesions, like those of the medial temporal lobe (MTL) cortex, disrupt item and word pair recognition, and that (2) hippocampal lesions disrupt temporal order memory and item recognition to the same degree. Not only was word pair recognition intact in the patient, but further evidence indicates that her recognition of other associations between items of the same kind is also spared so retrieval of such associations cannot be sufficient to support within-list temporal order recognition. Rather, as other evidence indicates that the patient is impaired at recognition of associations between different kinds of information, within-list (and possibly between-list) temporal order memory may be impaired by hippocampal lesions because it critically depends on retrieving associations between different kinds of information.

Factor analysis of three standardized tests of memory in a clinical population.

OBJECTIVES: The aim of this study was to determine the factor structure of three standardized memory tests: Wechsler Memory Scale-Revised (WMS-R), Warrington Recognition Memory Test (WRMT), Doors and People Test (D&P). We investigated whether these different standardized tests of memory are consistent in their evaluation of memory function, and the extent to which these tests discriminate between different memory functions (e.g. recall/recognition and verbal/non-verbal memory). DESIGN: Fifty patients with selective memory impairment were tested on the WMS-R, WRMT and D&P. METHODS: Age-scaled scores from selective measures of these tests (WMS-R-verbal, WMS-R-visual, WMS-R-delay, WRMT-words, WRMT-faces, D&P-people, D&P-doors, D&P-shapes, D&P-names) were used as input to a factor analysis. RESULTS: Maximum likelihood factor analysis yielded a three-factor solution consistent with a theoretically motivated fractionation of memory function into recall and recognition components. Recognition performance, but not recall performance, showed dissociation into visual and verbal components. CONCLUSIONS: The WMS-R, WRMT and D&P are highly consistent in their assessment of memory function. The results of the factor analysis are consistent with a theoretically motivated fractionation of recall and recognition memory. They are also partially consistent with a dissociation between visual and verbal memory function.

Does frontal lobe activation during retrieval reflect complexity of retrieved information?

Neuroimaging studies of memory have consistently shown that episodic retrieval is associated with right frontal activation, whereas semantic retrieval is associated with left frontal activation. Various hypotheses have been proposed to account for this lateralization in terms of underlying psychological processes. Alternatively, this lateralization may reflect the complexity of information retrieved: retrieval of complex, contextual information accompanying episodic retrieval invokes right-lateralized processes preferentially. We tested this hypothesis by manipulating the type and complexity of information retrieved. Initial increase in complexity of both episodic and semantic information was associated with right inferior frontal activation; further increase in complexity was associated with left dorsolateral activation. We conclude that frontal activation during retrieval is a non-linear function of the complexity of retrieved information.

Storage of verbal associations is sufficient to activate the left medial temporal lobe.

Neuroimaging studies have shown that memory encoding activates the medial temporal lobe (MTL). Many believe that these activations are related to novelty but it remains unproven which is critical - novelty detection or the rich associative encoding it triggers. We examined MTL activation during verbal associative encoding using functional magnetic resonance imaging. First, associative encoding activated left posterior MTL more than single word encoding even though novelty detection was matched, indicating not only that associative encoding activates the MTL particularly strongly, but also that activation does not require novelty detection. Moreover, it remains to be convincingly shown that novelty detection alone does produce such activation. Second, repetitive associative encoding produced less MTL activation than initial associative encoding, indicating that priming of associative information reduces MTL activation. Third, re-encoding familiar associations in a well-established way had a minimal effect on both memory and MTL activation, indicating that MTL activation reflects storage of associations, not merely their initial representation.

Are the benefits of errorless learning dependent on implicit memory?

The effectiveness of errorless and errorful learning methods was compared in two experiments in which a group of memory-impaired individuals learned lists of single words. In both experiments, error prevention during learning resulted in higher levels of cued recall performance than trial-and-error learning. Experiment 1 showed that the beneficial effects of the errorless learning method extended over a delay of up to 48 hr and were also observed in free recall. The hypothesis that the benefits of errorless learning rely upon implicit memory was tested in Experiment 2. No evidence was found to support the hypothesis. Implicit memory was observed following both errorless and errorful learning, but there was no indication that enhanced performance in the errorless condition could be accounted for by implicit memory. There was no correlation between performance on a direct test (cued recall) and performance on an indirect test (fragment completion) for the same materials. Furthermore, the extent of priming was no greater for recalled items than non-recalled items in the cued recall test. It is proposed that the benefits of errorless learning in this paradigm stem from the effects of error prevention on residual explicit memory.

Errorless learning of novel associations in amnesia.

In two experiments involving verbal association learning by people with memory impairments, the effectiveness of errorless learning (EL) was compared with errorful learning (EF). Experiment 1 examined the effectiveness of both methods in learning remotely linked word pairs. There was an advantage for items learned by EL at immediate test which was not sustained over a delay of 1 hr. Learning appeared to be stable over this delay in the EF condition. Analysis of responses at delayed cued recall showed more evidence of spontaneous recovery in EF than in EL. Elimination of these items from analysis resulted in a similar pattern of forgetting in both methods. Experiment 2 examined the effectiveness of EL and EF in teaching novel associations, and showed an advantage for EL at immediate and delayed test. Forgetting was apparently observed following EL, but not EF. As in Experiment 1, this discrepancy was attributed to recovered responses at delayed test in EF. Eliminating these responses showed a similar pattern of forgetting in both methods for items correctly recalled at immediate test. The study shows an advantage for EL techniques in learning novel associations. The two methods also differ in that learning via EF is associated with more spontaneous recovery.

The method of vanishing cues: an evaluation of its effectiveness in teaching memory-impaired individuals.

The method of vanishing cues and a standard rote learning method were used to teach a group of memory-impaired individuals a small computer vocabulary. Learning was observed using both teaching methods but no advantage was found for either one. A second experiment was carried out where modifications were made to the vanishing cues procedure in order to facilitate the use of implicit memory. Retention was significantly better following study with rote learning than with the modified vanishing cues procedure. A theoretical interpretation of these results and the reason for the failure to replicate previous findings is given.

Focal retrograde amnesia following closed head injury: a case study and theoretical account.

In this paper we present data from a closed head injury patient who presents a striking example of what Kapur (Cortex 29, 217-234, 1993) has termed " focal retrograde amnesia". The patient, D.H., is unable to recollect any autobiographical incidents from the pre-morbid period, although he is able to provide personal and public information from this period. The data are discussed in relation to other reported instances of focal retrograde amnesia and a preliminary theoretical account is offered.

Aetiological variation in the amnesic syndrome: comparisons using the list discrimination task.

In this study, the performance of amnesic patients with presumed temporal lobe damage was compared with that of patients with presumed diencephalic damage using the temporal list discrimination task. The two patient groups performed similarly on a measure of recognition, but the diencephalic group was impaired relative to the temporal lobe group on a measure of temporal discrimination. Discrimination performance in the temporal lobe group was significantly correlated with recognition memory. The data are interpreted as showing a qualitative difference in the form of amnesia arising from damage centred on the medial temporal lobes compared with that centred on the midline diencephalon.

Bilateral temporal lobe pathology with sparing of medial temporal lobe structures: lesion profile and pattern of memory disorder.

The lesion sustained by the amnesic patient H.M. consisted of bilateral ablation of medial temporal lobe structures with relative sparing of more lateral white matter and neocortical structures. We present the first detailed report of a case where the reverse pattern of lesions predominated, namely bilateral pathology of white matter and neocortical temporal lobe structures, with spared medial temporal lobe structures. This damage, which was particularly severe in anterior loci in the temporal lobes, was sustained as a result of radionecrosis. High-resolution magnetic resonance imaging was carried out to document the distinctive anatomical profile of our patient, and this profile was compared to that reported for the patient H.M. At the anatomical level, there was an almost "mirror image" profile, with contrasting involvement of lateral and medial temporal lobe structures. At the neuropsychological level, our patient was not amnesic but showed patchy impairment on traditional tests of anterograde memory functioning, in the context of notable "semantic" memory loss for knowledge acquired before and after the onset of his illness. Our findings demonstrate that bilateral temporal lobe pathology by itself does not lead to a classical amnesic syndrome, but may result in a significant but more subtle "semantic" memory loss. Our data highlight the distinctive and dissociable contribution of lateral and medial temporal lobe structures to human memory processing, and suggest a major role for anterior-inferior neocortical temporal lobe mechanisms in aspects of knowledge acquisition, storage and retrieval.