Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans?

The claim that recognition memory is spared relative to recall after focal hippocampal damage has been disputed in the literature. We examined this claim by investigating object and object-location recall and recognition memory in a patient, YR, who has adult-onset selective hippocampal damage. Our aim was to identify the conditions under which recognition was spared relative to recall in this patient. She showed unimpaired forced-choice object recognition but clearly impaired recall, even when her control subjects found the object recognition task to be numerically harder than the object recall task. However, on two other recognition tests, YR's performance was not relatively spared. First, she was clearly impaired at an equivalently difficult yes/no object recognition task, but only when targets and foils were very similar. Second, YR was clearly impaired at forced-choice recognition of object-location associations. This impairment was also unrelated to difficulty because this task was no more difficult than the forced-choice object recognition task for control subjects. The clear impairment of yes/no, but not of forced-choice, object recognition after focal hippocampal damage, when targets and foils are very similar, is predicted by the neural network-based Complementary Learning Systems model of recognition. This model postulates that recognition is mediated by hippocampally dependent recollection and cortically dependent familiarity; thus hippocampal damage should not impair item familiarity. The model postulates that familiarity is ineffective when very similar targets and foils are shown one at a time and subjects have to identify which items are old (yes/no recognition). In contrast, familiarity is effective in discriminating which of similar targets and foils, seen together, is old (forced-choice recognition). Independent evidence from the remember/know procedure also indicates that YR's familiarity is normal. The Complementary Learning Systems model can also accommodate the clear impairment of forced-choice object-location recognition memory if it incorporates the view that the most complete convergence of spatial and object information, represented in different cortical regions, occurs in the hippocampus.     

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.     

A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage

The spatial memory of a single patient (YR) was investigated. This patient, who had relatively selective bilateral hippocampal damage, showed the pattern of impaired recall but preserved item recognition on standardised memory tests that has been suggested by Aggleton and Shaw [Aggleton JP, Shaw C. Amnesia and recognition memory: a reanalysis of psychometric data. Neuropsychologia 1996;34:51-62] to be a consequence of Papez circuit lesions. YR was tested on three recall tests and one recognition test for visuospatial information. The initial recall test assessed visuospatial memory over very short unfilled delays and YR was not significantly impaired. This test was then modified to test recall of allocentric and egocentric spatial information separately after filled delays of between 5 and 60 s. YR was found to be more impaired at recalling allocentric than egocentric information after a 60 s interval with a tendency for the impairment to increase up to this delay. Recognition of allocentric spatial information was also assessed after delays of 5 and 60 s. YR was impaired after the 60 s delay. The results suggest that the human hippocampus has a greater involvement in allocentric than egocentric spatial memory, and that this most likely concerns the consolidation of allocentric information into long-term memory rather than the initial encoding of allocentric spatial information. The findings also suggest that YR's item recognition/free recall deficit pattern reflects a problem retrieving or storing certain kinds of associative information.     

Dissociation between recall and recognition memory performance in an amnesic patient with hippocampal damage following carbon monoxide poisoning

Some patients with relatively selective hippocampal damage have shown proportionate recall and recognition deficits. Moreover, familiarity as well as recollection have been found to be impaired in some of these patients. In contrast, other patients with apparently similar damage presented with relatively preserved recognition despite having severely impaired recall, and some of these patients have been shown to have preserved familiarity. We report here the case of an amnesic patient who suffered bilateral hippocampal damage and temporoparietal atrophy after carbon monoxide poisoning. On tests matched for difficulty, his recall performance was more severely impaired than his recognition memory, for verbal as well as for visual materials. Moreover, he performed within the range of healthy matched subjects on nine recognition tests out of ten. In a task using the process dissociation procedure, the patient's familiarity was preserved although his recollection was impaired. These findings indicate that recall and recognition memory can be dissociated in amnesic patients with hippocampal lesions even when temporoparietal cortical atrophy is also present.     

Recognition memory for single items and for associations in amnesic patients

Recognition memory performance reflects two distinct processes or types of memory referred to as recollection and familiarity. According to theoretical claims about the two types of memory, single item and associative recognition tasks can be used as an experimental method to distinguish recollection and familiarity processes. Associative recognition decisions can be used as an index of recollection while memory for single items is mostly based on familiarity judgement. We employed this procedure to examine a possible dissociation in the memory performance of amnesic patients between spared single item and impaired associative recognition. Twelve amnesic patients, six with damage confined to the hippocampus proper, and six with damage elsewhere in the brain, were recruited for the present study. The findings showed that hippocampal amnesics exhibit relative sparing of single item learning but are consistently deficient in the learning of all kinds of between-item associations. These results are consistent with the view that hippocampal formation contributes differently to declarative tasks that require recollective or familiarity processes.     

Recollection and familiarity in amnestic mild cognitive impairment: a global decline in recognition memory

Despite memory failures being a central feature of amnestic mild cognitive impairment (a-MCI), there is limited research into the nature of the memory impairment associated with this condition. A further understanding could lead to refinement of criteria needed to qualify for this designation and aid in prediction of who will progress to development of clinical Alzheimer's disease. Dual process models posit that recognition memory is supported by the dissociable processes of recollection and familiarity. The present study sought to evaluate recognition memory in a-MCI in the framework of the dual process model. Patients with a-MCI and age- and education-matched controls were tested on three memory paradigms. Two paradigms were modifications of the process-dissociation procedure in which recollection required either memory of word-pair associations (associative) or the font color of words at study (featural). A final paradigm utilized the task-dissociation methodology comparing performance for item and visual spatial source memory. All three tasks revealed that familiarity was impaired to at least the same extent as recollection. As familiarity is thought to be spared in normal aging, its measurement may provide a relatively specific marker for the early pathological changes of Alzheimer's disease.     

Contribution of familiarity and recollection to associative recognition memory: insights from event-related potentials

Within the dual-process perspective of recognition memory, it has been claimed that familiarity is sufficient to support recognition of single items, but recollection is necessary for associative recognition of item pairs. However, there are some reports suggesting that familiarity might support associative recognition judgments when the items form an easy to access bound representation. In contrast, recollection seems to be required for the recognition of bindings that might be flexibly rearranged in novel situations. We investigated whether both forms of binding are mediated by different mechanisms as reflected by a qualitatively different spatiotemporal eventrelated potential (ERP) pattern. In a recognition memory experiment, subjects gave old/new judgments to words learned by focusing either on interitem associations or on size relation of word triplets. Results revealed higher hit rates in the relational condition as compared to the associative condition. In addition, the proportion of triplets from which all three items were remembered was significantly larger in the relational condition suggesting that memory retrieval in this condition relies primarily on bound representations of word triplets. The ERP revealed a late parietal old/new effect for both conditions, with relational processing resulting in a greater effect. In contrast, an early frontal old/new effect was solely present in the associative condition. Taken together, these data provide evidence that familiarity might support associative recognition if the associated components are coherently encoded into a bound representation. Recollection might foster the recognition of relational bindings among items. This indicates that the contribution of familiarity and recollection to associative recognition depends on the kind of binding operations performed on the items rather than on the single versus multiple item distinction.     

Faces are special but not too special: Spared face recognition in amnesia is based on familiarity

Most current theories of human memory are material-general in the sense that they assume that the medial temporal lobe (MTL) is important for retrieving the details of prior events, regardless of the specific type of materials. Recent studies of amnesia have challenged the material-general assumption by suggesting that the MTL may be necessary for remembering words, but is not involved in remembering faces. We examined recognition memory for faces and words in a group of amnesic patients, which included hypoxic patients and patients with extensive left or right MTL lesions. Recognition confidence judgments were used to plot receiver operating characteristics (ROCs) in order to more fully quantify recognition performance and to estimate the contributions of recollection and familiarity. Consistent with the extant literature, an analysis of overall recognition accuracy showed that the patients were impaired at word memory but had spared face memory. However, the ROC analysis indicated that the patients were generally impaired at high confidence recognition responses for faces and words, and they exhibited significant recollection impairments for both types of materials. Familiarity for faces was preserved in all patients, but extensive left MTL damage impaired familiarity for words. These results show that face recognition may appear to be spared because performance tends to rely heavily on familiarity, a process that is relatively well preserved in amnesia. In addition, the findings challenge material-general theories of memory, and suggest that both material and process are important determinants of memory performance in amnesia.     

Associative reinstatement: A novel approach to assessing associative memory in patients with unilateral temporal lobe excisions

We investigated whether unilateral medial temporal lobe (MTL) damage disrupts associative reinstatement, which represents the gain in item memory when the studied associative information is reinstated at retrieval. We were interested to see whether associative reinstatement relies on the same relational binding operations that support other types of associative memory (associative identification and recollection) thought to be subserved by the MTL. In addition, we examined whether such damage affects the different types of associative memory to a greater extent than item memory and item familiarity, and whether a different pattern is seen in patients with language dominant relative to non-dominant temporal lobe resection when the studied material consists of verbal information. To do so, we used a word pair recognition paradigm composed of two tasks: (1) a pair recognition task that provides measures of associative reinstatement and item memory, and (2) an associative identification recognition task that provides a measure of associative identification memory. Estimates of item familiarity and recollection were derived from performance on both tasks using a variant of the process-dissociation procedure. Our results showed that associative reinstatement, like other types of associative memory measures, was impaired in patients with unilateral resection, irrespective of the side of damage. Item familiarity, however, was impaired solely following language dominant resection. The lack of a laterality effect in our relational measures was likely due to using an encoding task that promoted formation of both verbal and visual associations, whereas item-based familiarity could rely exclusively on verbal operations. We propose that associative reinstatement provides a sensitive measure of relational memory that is less dependent on strategic processing and therefore more appropriate for evaluating MTL function in patients.     

Impact of novelty and type of material on recognition in healthy older adults and persons with mild cognitive impairment

The goal of this study was to assess the effect of novelty on correct recognition (hit minus false alarms) and on recollection and familiarity processes in normal aging and amnestic mild cognitive impairment (MCI). Recognition tasks compared well-known and novel stimuli in the verbal domain (words vs. pseudowords) and in the musical domain (well-known vs. novel melodies). Results indicated that novel materials associated with lower correct recognition and lower recollection, an effect that can be related to its lower amenability to elaborative encoding in comparison with well-known items. Results also indicated that normal aging impairs recognition of well-known items, whereas MCI impairs recognition of novel items only. Healthy older adults showed impaired recollection and familiarity relative to younger controls and individuals with MCI showed impaired recollection relative to healthy older adults. The recollection deficit in healthy older adults and persons with MCI and their impaired recognition of well-known items is compatible with the difficulty both groups have in encoding information in an elaborate manner. In turn, familiarity deficit could be related to impaired frontal functioning. Therefore, novelty of material has a differential impact on recognition in persons with age-related memory disorders.     

Preserved visual recognition memory in an amnesic patient with hippocampal lesions

There is ongoing debate about whether performance on tests of recognition memory can remain preserved after hippocampal damage. In the present study, we report F.R.G., a patient who became severely amnesic following herpes simplex encephalitis. Although F.R.G. failed all tests involving recall and verbal recognition, she obtained normal performance on a wide number of tests evaluating visual recognition memory (14 of 18 different tests). Her performance was independent of various factors, such as test difficulty, duration of exposure to the stimuli, or delay separating encoding and recognition. F.R.G. also achieved normal performance on two tasks requiring that she associate pairs of visual stimuli. In addition, she demonstrated spared feeling of knowing, suggesting that her performance on recognition tests was explicit and likely to rely on familiarity. Brain imaging (MRI) revealed bilateral lesions of the hippocampus and lesions of the left parahippocampal gyrus, while the right parahippocampal gyrus remained relatively spared. The results of this study support the view that recognition memory can be preserved despite severe hippocampal damage and that familiarity is a distinct memory process that can be dissociated from recollection.     

Intact suppression of increased false recognition in schizophrenia

OBJECTIVE: Recognition memory is impaired in patients with schizophrenia, as they rely largely on item familiarity, rather than conscious recollection, to make mnemonic decisions. False recognition of novel items (foils) is increased in schizophrenia and may relate to this deficit in conscious recollection. By studying pictures of the target word during encoding, healthy adults can suppress false recognition. This study examined the effect of pictorial encoding on subsequent recognition of repeated foils in patients with schizophrenia. METHOD: The study included 40 patients with schizophrenia and 32 healthy comparison subjects. After incidental encoding of 60 words or pictures, subjects were tested for recognition of target items intermixed with 60 new foils. These new foils were subsequently repeated following either a two- or 24-word delay. Subjects were instructed to label these repeated foils as new and not to mistake them for old target words. RESULTS: Schizophrenic patients showed greater overall false recognition of repeated foils. The rate of false recognition of repeated foils was lower after picture encoding than after word encoding. Despite higher levels of false recognition of repeated new items, patients and comparison subjects demonstrated a similar degree of false recognition suppression after picture, as compared to word, encoding. CONCLUSIONS: Patients with schizophrenia displayed greater false recognition of repeated foils than comparison subjects, suggesting both a decrement of item- (or source-) specific recollection and a consequent reliance on familiarity in schizophrenia. Despite these deficits, presenting pictorial information at encoding allowed schizophrenic subjects to suppress false recognition to a similar degree as the comparison group, implying the intact use of a high-level cognitive strategy in this population.     

Effect of unitization on associative recognition in amnesia

We examined how associative recognition performance in amnesic patients is mediated by use of a unitized (i.e., holistic) encoding strategy, and the degree to which the unitization effect is related to sparing of familiarity-based recognition. Participants studied word pairs as either separate lexical units in sentences (i.e., nonunitized) or as compounds (unitized). Under standard recognition instructions, normal controls and patients with left-temporal lobe damage (previously determined to have impairments in both recollection and familiarity) showed no difference for unitized and nonunitized pairs, whereas hypoxics (previously determined to have impaired recollection but relatively preserved familiarity) showed an advantage of unitized over nonunitized pairs. This effect was reproduced in normal healthy participants under instructions to restrict responses to judgments of familiarity. The results indicate that unitization may mediate the degree of associative recognition impairment exhibited by some amnesic patients, and that the effect is related to preserved familiarity capacity. The relevance of the results to the debate over the importance of the hippocampus in memory for associations is discussed.     

Fractionation of memory in medial temporal lobe amnesia

We report a comprehensive investigation of the anterograde memory functions of two patients with memory impairments (RH and JC). RH had neuroradiological evidence of apparently selective right-sided hippocampal damage and an intact cognitive profile apart from selective memory impairments. JC, had neuroradiological evidence of bilateral hippocampal damage following anoxia due to cardiac arrest. He had anomic and "executive" difficulties in addition to a global amnesia, suggesting atrophy extending beyond hippocampal regions. Their performance is compared with that of a previously reported hippocampal amnesic patient who showed preserved recollection and familiarity for faces in the context of severe verbal and topographical memory impairment [VC; Cipolotti, L., Bird, C., Good, T., Macmanus, D., Rudge, P., & Shallice, T. (2006). Recollection and familiarity in dense hippocampal amnesia: A case study. Neuropsychologia, 44, 489-506.] The patients were administered experimental tests using verbal (words) and two types of non-verbal materials (faces and buildings). Receiver operating characteristic analyses were used to estimate the contribution of recollection and familiarity to recognition performance on the experimental tests. RH had preserved verbal recognition memory. Interestingly, her face recognition memory was also spared, whilst topographical recognition memory was impaired. JC was impaired for all types of verbal and non-verbal materials. In both patients, deficits in recollection were invariably associated with deficits in familiarity. JC's data demonstrate the need for a comprehensive cognitive investigation in patients with apparently selective hippocampal damage following anoxia. The data from RH suggest that the right hippocampus is necessary for recollection and familiarity for topographical materials, whilst the left hippocampus is sufficient to underpin these processes for at least some types of verbal materials. Face recognition memory may be adequately subserved by areas outside of the hippocampus.     

Event-related potentials associated with masked priming of test cues reveal multiple potential contributions to recognition memory

The relationship between recognition memory and repetition priming remains unclear. Priming is believed to reflect increased processing fluency for previously studied items relative to new items. Manipulations that affect fluency can also affect the likelihood that participants will judge items as studied in recognition tasks. This attribution of fluency to memory has been related to the familiarity process, as distinct from the recollection process, that is assumed by dual-process models of recognition memory. To investigate the time courses and neural sources of fluency, familiarity, and recollection, we conducted an event-related potential (ERP) study of recognition memory using masked priming of test cues and a remember/know paradigm. During the recognition test, studied and unstudied words were preceded by a brief, masked word that was either the same or different. Participants decided quickly whether each item had been studied ("old" or "new"), and for items called old, indicated whether they "remembered" (R) the encoding event, or simply "knew" (K) the item had been studied. Masked priming increased the proportion of K, but not R, judgments. Priming also decreased response times for hits but not correct rejections (CRs). Four distinct ERP effects were found. A medial-frontal FN400 (300-500 msec) was associated with familiarity (R, K Hits > CRs) and a centro-parietal late positivity (500-800 msec) with recollection (R Hits > K Hits, CRs). A long-term repetition effect was found for studied items judged "new" (Misses > CRs) in the same time window as the FN400, but with a posterior distribution. Finally, a centrally distributed masked priming effect was visible between 150 and 250 msec and continued into the 300-500 msec time window, where it was topographically dissociable from the FN400. These results suggest that multiple neural signals are associated with repetition and potentially contribute to recognition memory.     

Assessing Recollection and Familiarity in Autistic Spectrum Disorders: Methods and Findings

We hypothesise that of the two processes underlying declarative memory, recollection is impaired in high-functioning autism (HFA) whereas recollection and familiarity are impaired in low-functioning autism (LFA). Testing these hypotheses necessitates assessing recollection and familiarity separately. However, this is difficult, because both processes contribute to performance on standard memory tests. Moreover, tests must be suitable for use with young or intellectually disabled participants. This study aimed to develop tests of recollection and familiarity separately, and to make preliminary tests of our hypotheses. We developed a temporal source memory task to assess recollection in LFA, and a shape recognition task to assess familiarity and an action recall task assessing recollection in HFA. The methods and implications of the results are discussed.     

The role of recollection and familiarity in the functional differentiation of the medial temporal lobes

The components of the medial temporal lobes (MTL) receive different kinds of input. The perirhinal cortex receives primarily object/item information, the parahippocampal cortex receives contextual information, and the hippocampus receives high-level inputs that include object/item, context, and other information. Critically, the perirhinal and parahippocampal cortices have similar cytoarchitectonics, which differ considerably from that of the hippocampus and suggest that these cortices process their inputs differently from the way that the hippocampus processes its inputs. Much evidence indicates that the hippocampus is designed to rapidly bind together pattern-separated representations that support recall/recollection well. In contrast, the newer MTL cortices rapidly create poorly pattern-separated memories that support familiarity well, but recall/recollection very poorly. For over a decade, there has been disagreement about whether recall/recollection is primarily mediated by the hippocampus and familiarity by the evolutionarily newer MTL cortices or whether the MTL mediates these kinds of memory in an integrated, homogeneous fashion. Common misconceptions about familiarity, recollection, item, and associative memory are discussed as are methodological problems with MTL lesion and functional imaging research. The possible confound of familiarity with weaker memory and recollection with stronger memory is discussed and the implications of the Montaldi et al. (2006) functional Magnetic Resonance Imaging (fMRI) study, which matched memory strength between strong familiarity and recollection, finding that only recollection activated the hippocampus, are discussed. A suggestion is made about how the long-running conflict of findings in the human hippocampal lesion literature may be resolved.     

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.     

Using ERPs to dissociate recollection from familiarity in picture recognition

Dual process theories posit that separate recollection and familiarity processes contribute to recognition memory. Previous research, testing recognition memory for words, indicates that event-related brain potentials (ERPs) can be used to dissociate recollection from familiarity. It has been hypothesized that the FN400 ERP old/new effect (300-500 ms) varies with stimulus familiarity, but the parietal ERP old/new effect (400-800 ms) varies with recollection. The results reported here are consistent with this hypothesis, extending it to the recognition of pictures when subjects had to discriminate between studied pictures, highly familiar lures (mirror-reversals of studied pictures), and new pictures. Furthermore, the parietal old/new effect showed significant recollection-related differences only for subjects with good behavioral discrimination between studied items and similar lures.     

Familiarity in source memory

Familiarity and recollection are thought to be separate processes underlying recognition memory. Event-related potentials (ERPs) dissociate these processes, with an early (approximately 300-500ms) frontal effect relating to familiarity (the FN400) and a later (500-800ms) parietal old/new effect relating to recollection. It has been debated whether source information for a studied item (i.e., contextual associations from when the item was previously encountered) is only accessible through recollection, or whether familiarity can contribute to successful source recognition. It has been shown that familiarity can assist in perceptual source monitoring when the source attribute is an intrinsic property of the item (e.g., an object's surface color), but few studies have examined its contribution to recognizing extrinsic source associations. Extrinsic source associations were examined in three experiments involving memory judgments for pictures of common objects. In Experiment 1, source information was spatial and results suggested that familiarity contributed to accurate source recognition: the FN400 ERP component showed a source accuracy effect, and source accuracy was above chance for items judged to only feel familiar. Source information in Experiment 2 was an extrinsic color association; source accuracy was at chance for familiar items and the FN400 did not differ between correct and incorrect source judgments. Experiment 3 replicated the results using a within-subjects manipulation of spatial vs. color source. Overall, the results suggest that familiarity's contribution to extrinsic source monitoring depends on the type of source information being remembered.