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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.

Adult↗

The cannabinoid agonist WIN 55,212-2 reduces sensorimotor gating and recognition memory in rats.

Cannabinoids can disrupt short-term memory in humans and animals and induce learning deficits and other cognitive impairments. In the present study we examined the role of a full cannabinoid agonist in short-term memory, sensorimotor gating, and the acquisition and expression of an operant learning paradigm in rats. We tested the effects of the synthetic cannabinoid WIN 55,212-2 (0.6 and 1.2 mg/kg) on short-term memory in social and object recognition tests, on prepulse inhibition (PPI) of startle, as well as on lever pressing for palatable food. Injections of 0.6 and 1.2 mg/kg WIN 55,212-2 impaired recognition memory and PPI in a dose-dependent manner, but had no effect on lever-pressing acquisition or expression, or on food preference. The PPI deficit was reversed by the administration of 0.1 mg/kg haloperidol. These data suggest that the synthetic cannabinoid WIN 55,212-2 does not lead to a general impairment of learning in an appetitive instrumental task, but significantly affects short-term memory and sensorimotor integration. The impairment in recognition and PPI might be due to deficits in attention-based short-term information processing.

Animals↗

Benzodiazepine impairment of perirhinal cortical plasticity and recognition memory.

Benzodiazepines, including lorazepam, are widely used in human medicine as anxiolytics or sedatives, and at higher doses can produce amnesia. Here we demonstrate that in rats lorazepam impairs both recognition memory and synaptic plastic processes (long-term depression and long-term potentiation). Both impairments are produced by actions in perirhinal cortex. The findings thus establish a mechanism by means of which benzodiazepines impair recognition memory. The findings also strengthen the hypotheses that the familiarity discrimination component of recognition memory is dependent on reductions in perirhinal neuronal responses when stimuli are repeated and that these response reductions are due to a plastic mechanism also used in long-term depression.

Animals↗

Sensory and semantic factors in recognition memory for odors and graphic stimuli: elderly versus young persons.

In four experiments, young (18-26 years, M = 21) and elderly (over 65 years, M = 72) people were compared for recognition memory of (a) graphic stimuli (faces of presidents and vice presidents, engineering symbols, and free forms) and (b) everyday odors. On graphic stimuli, the elderly consistently matched the young, but on odors the performance of the elderly was worse. Their poorer olfactory performance was observed after only 26 s, but became truly marked after 1 hr or more. Somewhere between 1 hr and 2 weeks, their odor performance fell to chance, but their graphic performance remained well above chance. Although the young did forget both graphic and odor materials progressively, their performance always stayed above chance over a 6-month period. Experiments 1 and 2 revealed that the elderly are less sensitive to odors than the young (with thresholds about 10-fold higher), which may explain, in part, their poorer olfactory memory performance. Knowledge that the subjects brought to the tasks by way of familiarity with and ability to name odors and faces played a positive role in recognition memory. Because of this positive role, together with the negative role played by verbal distraction, we conclude that odor recognition memory depends, perhaps heavily, on semantic processing. Impaired semantic processing may result even when odors are simply rendered desaturated, or pastel because of the weakening of olfactory sensitivity with aging.

Adolescent↗

Recall and recognition memory in Parkinson's disease.

This study is concerned with recall and recognition memory in patients with Parkinson's disease. The results show that the Parkinson group was significantly impaired on tests of free recall compared to a group of age matched controls. By contrast, when given tests of recognition memory for the same items their performance was practically identical. In recall, significant main effects are reported for serial position and list presentation but no qualitative differences were observed between the two groups on these measures, both of which showed a primacy and recency effect. However, the control subjects recalled significantly more words in their original order of presentation than the patient group, a difference which appears to have occurred at the level of input. It was concluded that although the patient group was able to adopt and use similar strategies to the control subjects, they were less efficient in using these, a difficulty which was attributed to limited capacity due to mental slowness.

Aged↗

The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys.

Recognition memory was assessed by submitting the same adult monkeys to visual paired comparison (VPC) with mixed delays (10-120 sec), followed by three consecutive versions of object-delayed nonmatching-to-sample (DNMS): increasing delays (10-600 sec), lengthened lists (3-10 objects), and intervening distractors in the delays (light at 10 sec, motor task at 30-600 sec, or context change at 600 sec). Four groups were tested: normal controls, monkeys with ibotenic acid lesions of the hippocampal formation (H), and monkeys with aspiration lesions of either the perirhinal (PRh) or parahippocampal (areas TH/TF) cortex. Group H was impaired on VPC at delays > or =60 sec but had difficulty on DNMS only at 600 sec delays with distraction. In group TH/TF, the VPC impairment emerged earlier (30 sec); yet, once the nonmatching rule was mastered, no significant change occurred on any DNMS condition. Only group PRh behaved congruently on VPC and DNMS, exhibiting a deficit at the easiest condition that worsened with increasing delays as well as in DNMS lengthened list and distraction conditions. These results led us to postulate that VPC and DNMS, as previously administered to monkeys, were not equivalent visual recognition memory probes. Specifically, we propose that, for VPC, because of passive (incidental) encoding, the animal's performance rests on both item familiarity and event recollection, whereas, for DNMS, because of active (purposeful) encoding, performance relies more on item familiarity. This proposal converges with current models postulating distinct, but interactive, mnemonic roles for the hippocampal and adjacent TH/TF regions.

Animals↗

Turning up the noise or turning down the volume? On the nature of the impairment of episodic recognition memory by midazolam.

E. Hirshman, J. Fisher, T. Henthom, J. Amdt, and A. Passanname (2002) found that Midazolam disrupts the mirror-patterned word-frequency effect for recognition memory by reversing the typical hit-rate advantage for low-frequency words. They noted that this result is consistent with dual-process accounts (e.g., R. C. Atkinson & J. F. Juola, 1974; G. Mandler, 1980; A. P. Yonelinas, 1994) of the word frequency effect for recognition memory (S. Joordens & W. E. Hockley. 2000; L. M. Reder et al. 2000). The present authors show that this finding is also consistent with a variety of single-process, retrieving effectively- from-memory (REM) models (R. M. Shiffrin & M. Steyvers, 1997), the simplest of which assumes that Midazolam decreases the accuracy with which memory traces are stored. These findings therefore do not discriminate between single- and dual-process models of recognition memory.

Attention↗

Bilateral thalamic lesions affect recollection- and familiarity-based recognition memory judgments.

The contribution of the thalamus to different forms of explicit memory is poorly understood. In the current study, explicit memory performance was examined in a 40-year-old male (RG) with bilateral anterior and medial thalamic lesions. Standardized tests indicated that the patient exhibited more severe recall than recognition deficits and his performance was generally worse for verbal compared to nonverbal memory. Recognition memory tests using the remember-know (R/K) procedure and the confidence-based receiver operating characteristic (ROC) procedure were used to examine recollection- and familiarity-based recognition. These tests revealed that RG had deficits in recollection and smaller, but consistent deficits in familiarity. The results are in agreement with models indicating that the anteromedial thalamus is important for both recollection- and familiarity-based recognition memory.

Adult↗

Recognition memory deficits in a subpopulation of aged monkeys resemble the effects of medial temporal lobe damage.

The present study examined individual differences in recognition memory function in a group of Old World monkeys (Macaca mulatta). Four young (9-11 years) and 10 aged (22-33 years) monkeys were tested in the same delayed-nonmatching-to-sample (DNMS) recognition memory procedure that has been widely used to study the effects of experimental hippocampal lesions in young subjects. Animals were first trained to a 90% correct learning criterion in the DNMS task using a 10-second delay between the sample and recognition phase of each trial. The memory demands of the task were then increased by gradually extending the retention interval from 15 seconds to 10 minutes. Three of the aged monkeys performed as accurately as young subjects at all delays. The remaining aged monkeys performed well at the shortest delays (15 and 30 seconds), but progressively greater impairments emerged across delays of 60 seconds, 2 minutes, and 10 minutes. These results suggest that recognition memory is only compromised in a subpopulation of aged monkeys. Moreover, aged monkeys that are impaired in the DNMS task exhibit the same delay-dependent pattern of deficits that is the hallmark of memory dysfunction resulting from medial temporal lobe damage.

Aging↗

Impaired facial recognition memory in aging and dementia.

Young normals, aged normals, and patients with early and advanced probable dementia of the Alzheimer type (DAT) were administered a facial recognition memory task. A continuous recognition paradigm was used, in which subjects were instructed to identify the repeated faces in an ongoing series of faces presented on a video monitor screen. A signal detection analysis of the data revealed that the DAT patients were markedly impaired in their ability to discriminate between new and repeated faces. Multiple presentations of faces improved the recognition accuracy of the early DAT patients only, but their rate of learning was slower than that of the normal subjects. In comparison to the young normals, elderly normals exhibited a mild deficit in recognition memory. All of the elderly subject groups exhibited a more liberal response bias than the young normals, which eliminates the possibility that the impaired memory task performance of the aged subjects could be attributed to a more conservative test-taking strategy. The DAT patients exhibited impaired recognition even when the second presentation of a face immediately followed the first, which perhaps implies that task performance was also sensitive to the effect of DAT on visuoperceptual abilities or psychomotor speed.

Adolescent↗

Amnesia and recognition memory: a re-analysis of psychometric data.

The present study compared the recognition memory deficit in different groups of amnesics using scores from a standard test. The data, taken from a literature search, came from 33 studies reporting the performance of amnesic subjects on the recognition memory test (RMT) [77]. A total of 112 amnesic subjects were grouped according to their pathology. In addition, the analysis included subjects with schizophrenia, amygdala damage, or frontal lobe damage. Of these three nonamnesic groups, only the frontal lobe subjects were impaired on both RMT subtests, while the schizophrenics showed a disproportionate impairment for the recognition of faces. The amygdala subjects were also poor at face recognition. Among the amnesic groups, those subjects likely to have multiple sites of pathology (e.g. Korsakoff amnesics, post-encephalitics) were found to be the most impaired on the RMT. In contrast, those amnesics with more focal, limbic lesions in the hippocampus, fornix, or mamillary body region showed much milder deficits on the RMT task, some performing at normal levels. Despite their apparent sparing of recognition, the overall severity of amnesia in those subjects with limbic lesions appeared comparable to that in the remaining amnesics. These findings indicate that deficits on both subtests of the RMT are a frequent but not inevitable component of anterograde amnesia. They also point to a distinct subgroup of amnesias associated with selective damage in the hippocampus or its diencephalic targets, in which there is a relative sparing of recognition under certain test conditions.

Adolescent↗

Recognition memory for words and event-related potentials: a comparison of normal and disabled readers.

Visual event-related potentials elicited during a word-recognition memory task were examined for groups of normal and disabled readers (RD). The strong association of reading ability with recognition memory performance endorsed the appropriateness of this signal detection paradigm as a reading-related task. Enhanced amplitude of the P200 component for the RD group was evident during both the acquisition and recognition series and it is indicative of differences at an early sensory stage of item encoding and retrieval. Normal readers displayed greater N400 amplitude than the RD group during both the acquisition and recognition series, an effect which is consistent with more extensive semantic evaluation or memory search that is attributed to that component. In the absence of any remarkable differences in P300 amplitude between groups, the poorer recognition memory performance for the RD group may not be attributable to attentional deficits.

Child↗

Impaired recognition memory in rats after damage to the hippocampus.

Rats with radio-frequency or ibotenic acid lesions of the hippocampus and rats with radio-frequency lesions of the fornix were tested on the visual paired comparison task (VPC), a test of recognition memory. Memory was assessed at five different delay intervals ranging from 10 sec to 24 hr. All operated groups performed normally at the shorter delays (10 sec and 1 min). Across longer delays, the two groups with hippocampal damage were impaired. Rats with fornix lesions performed well on the VPC task but were impaired on a spatial task (spontaneous alternation). The results show that the hippocampus is essential for normal recognition memory. Moreover, fornix lesions need not mimic the effects of direct damage to hippocampal tissue. The findings are discussed in the context of the contribution of the hippocampus to recognition memory.

Animals↗

Functional MRI and novel picture-learning among older patients with chronic schizophrenia: abnormal correlations between recognition memory and medial temporal brain response.

The relationship between disordered brain function and learning deficits in chronic schizophrenia is unclear. The authors compared correlations of brain response to picture encoding with subsequent recognition memory between samples of clinically stable patients over age 45 with schizophrenia and demographically similar healthy individuals. Subjects were studied with functional magnetic resonance imaging during novel picture encoding and a control condition. Comparison subjects showed an inverse relationship between subsequent recognition memory and brain response in medial temporal areas. Among schizophrenia patients, brain response in these regions was positively correlated with recognition memory. Brain-behavior relationships during learning were thus found to be qualitatively different between schizophrenic patients and healthy subjects.

Aged↗

Recognition memory of newly learned faces.

We used event-related fMRI to study recognition memory of newly learned faces. Caucasian subjects memorized unfamiliar, neutral and happy South Korean faces and 4 days later performed a memory retrieval task in the MR scanner. We predicted that previously seen faces would be recognized faster and more accurately and would elicit stronger neural activation than novel faces. Consistent with our hypothesis, novel faces were recognized more slowly and less accurately than previously seen faces. We found activation in a distributed cortical network that included face-responsive regions in the visual cortex, parietal and prefrontal regions, and the hippocampus. Within all regions, correctly recognized, previously seen faces evoked stronger activation than novel faces. Additionally, in parietal and prefrontal cortices, stronger activation was observed during correct than incorrect trials. Finally, in the hippocampus, false alarms to happy faces elicited stronger responses than false alarms to neutral faces. Our findings suggest that face recognition memory is mediated by stimulus-specific representations stored in extrastriate regions; parietal and prefrontal regions where old and new items are classified; and the hippocampus where veridical memory traces are recovered.

Adult↗

The effect of item sequence on brain activity during recognition memory.

Two basic types of experimental designs are available to measure the brain indices of successful recognition memory. Both designs have in common that brain activity elicited by correctly recognized studied (old) items is compared to brain activity elicited by correctly rejected new items. In blocked designs, the two item types are presented in separate lists. In random-mixed designs, on the other hand, they are randomly intermixed within the same list. Early studies reported that in random-mixed designs, brain activity can be affected by the sequence in which different types of items are presented. Here, we investigated to what extent such sequence effects also occur in random-mixed designs of recognition memory. Event-related potentials (ERPs) were obtained while subjects made recognition judgments on pseudorandom sequences of visually presented new and old words. Changes in the sequence from one item-type to another (change from old to new and from new to old) were associated with a prominent P300 potential for new words following old words but not vice versa. Subjects with larger P300 potentials made less false alarms to such new words. Successive presentations of the same item-type (sequence 'blocks': three old words in a row and three new words in row) were associated with a left parietal positive slow shift for successive old words but not for successive new words. The data suggest that new words require extensive context-updating if they are presented within the context generated by preceding old words. Due to these sequence effects, the present data question the assumption that random-mixed designs are generally favorable over block designs.

Adult↗

The glycine/NMDA receptor antagonist HA-966 impairs visual recognition memory in rhesus monkeys.

Recent studies have shown that strychnine-insensitive glycine binding sites positively modulate the N-methyl-D-asparate (NMDA) subclass of glutamate receptors, which are important in neural pathways involved in cognitive function. We examined the effect of (+/-)-3-amino-1-hydroxy-2-pyrrolidone (HA-966), a highly specific antagonist of this glycine modulatory site on the NMDA receptor, on visual recognition memory in four rhesus monkeys performing a computer-automated version of delayed nonmatching-to-sample (DNMS) with a list length of 20 trial-unique graphic symbols. In addition, the effect of HA-966 was compared with that of (+)-5-methyl-10, 11-dihydro-5H-dibenzo[a,d]cyclohepten-5, 10-imine (dizocilpine; MK-801), a noncompetitive NMDA channel blocker. Administration of HA-966 (0.1-10 mg/kg, i.m.) 30 min before testing impaired DNMS performance dose-dependently, starting at doses of 3.2 mg/kg; the memory deficity following the highest dose (10 mg/kg) was associated with prolonged response latencies. Similar impairments in recognition memory were observed following treatment with MK-801, though at much lower doses (3.2-32 micrograms/kg) than those at which HA-966 was effective. Administration of low doses of HA-966 (1 mg/kg) and MK-801 (10 micrograms/kg), each of which had no significant effect on performance when given alone, also failed to impair performance when given concurrently. Combined administration of both drugs, each at amnesia-producing doses (3.2 mg/kg of HA-966 plus 32 micrograms/kg of MK-801), markedly impaired performance in an additive, not a synergistic, manner. From these results, we propose that the recognition memory impairment observed in our monkeys following HA-966 administration is via an action on the glycine modulatory site of the NMDA receptor complex.

Animals↗

Word imageability affects the hippocampus in recognition memory.

Concrete words, whose meanings are readily imagined, are better remembered than abstract words. However, the neural correlates of this effect are poorly understood. Here, we investigated the effect of imageability on brain activity in the medial temporal lobe (MTL) processes underlying recognition memory. We recorded event-related potentials (ERPs) via depth electrodes from within the MTL in 14 patients with drug-resistant epilepsy. Patients performed a continuous word recognition task with words of high and low imageability (controlled for word frequency). Behaviorally, recognition performance was better for high, compared to low, imageable words. Two ERP components associated with recognition memory, the AMTL-N400 and the hippocampal late negative component, showed an old/new effect, but only the hippocampal P600 showed a main effect of imageability. We suggest that the hippocampal effect of imageability in recognition memory may be associated with conceptual or pictorial information processing of concrete words.

Adult↗