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Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex.

Recordings of the activity of 2705 single neurones were made in entorhinal and perirhinal cortex, area TG of the temporal lobe, and the inferior temporal cortex both during monkeys' performance of a serial recognition memory task using complex pictures and when monkeys were shown objects. Responses of 120 (9.7%) of the visually responsive neurons recorded were significantly smaller to the second than to the first presentations of unfamiliar stimuli. The incidence of such responses was highest in perirhinal cortex plus areas TE1 and TE2 of the temporal lobe, intermediate in lateral entorhinal cortex and areas TE3 and TG, and lowest in other parts of entorhinal and inferior temporal cortex. Response decrements were maintained across 20 or more intervening presentations of other stimuli for the majority of the neurones tested. Responses of 43 (14.4%) of the visually responsive neurones tested were significantly greater to unfamiliar than to highly familiar stimuli. Such differential responses were found only in lateral entorhinal and perirhinal cortex plus areas TG, TE1, TE2 and TE3. For 6 neurones the response difference was significant even when the familiar stimuli had not been seen for more than 24 h: such neurones demonstrate access to information stored in long-term memory for more than 24 h. Seven familiarity neurones signalled information concerning the relative familiarity of stimuli but not information concerning how recently they were last seen; 58 recency neurones signalled information concerning the recency of presentation of stimuli, but not their relative familiarity. Thus certain neurones demonstrate the separable encoding of recency and familiarity information. Neurones signalling information of use for recognition memory are found in cortex close to the rhinal sulcus where lesions result in major deficits in the performance of recognition memory tasks. The conjunction of these findings provides strong evidence for the importance of these neurones and this cortex for processes (recency and familiarity discrimination) necessary for recognition and working memory. The possible relation of the neuronal responses to priming memory is also discussed.

Animals↗

Pragmatics of measuring recognition memory: applications to dementia and amnesia.

This article has two purposes. The first is to describe four theoretical models of yes-no recognition memory and present their associated measures of discrimination and response bias. These models are then applied to a set of data from normal subjects to determine which pairs of discrimination and bias indices show independence between discrimination and bias. The following models demonstrated independence: a two-high-threshold model, a signal detection model with normal distributions using d' and C (rather than beta), and a signal detection model with logistic distributions and a bias measure analogous to C. C is defined as the distance of criterion from the intersection of the two underlying distributions. The second purpose is to use the indices from the acceptable models to characterize recognition memory deficits in dementia and amnesia. Young normal subjects, Alzheimer's disease patients, and parkinsonian dementia patients were tested with picture recognition tasks with repeated study-test trials. Huntington's disease patients, mixed etiology amnesics, and age-matched normals were tested by Butters, Wolfe, Martone, Granholm, and Cermak (1985) using the same paradigm with word stimuli. Demented and amnesic patients produced distinctly different patterns of abnormal memory performance. Both groups of demented patients showed poor discrimination and abnormally liberal response bias for words (Huntington's disease) and pictures (Alzheimer's disease and parkinsonian dementia), whereas the amnesic patients showed the worst discrimination but normal response bias for words. Although both signal detection theory and two-high-threshold discrimination parameters showed identical results, the bias measure from the two-high-threshold model was more sensitive to change than the bias measure (C) from signal detection theory. Three major points are emphasized. First, any index of recognition memory performance assumes an underlying model. Second, even acceptable models can lead to different conclusions about patterns of learning and forgetting. Third, efforts to characterize and ameliorate abnormal memory should address both discrimination and bias deficits.

Adult↗

Investigation of facial recognition memory and happy and sad facial expression perception: an fMRI study.

We investigated facial recognition memory (for previously unfamiliar faces) and facial expression perception with functional magnetic resonance imaging (fMRI). Eight healthy, right-handed volunteers participated. For the facial recognition task, subjects made a decision as to the familiarity of each of 50 faces (25 previously viewed; 25 novel). We detected signal increase in the right middle temporal gyrus and left prefrontal cortex during presentation of familiar faces, and in several brain regions, including bilateral posterior cingulate gyri, bilateral insulae and right middle occipital cortex during presentation of unfamiliar faces. Standard facial expressions of emotion were used as stimuli in two further tasks of facial expression perception. In the first task, subjects were presented with alternating happy and neutral faces; in the second task, subjects were presented with alternating sad and neutral faces. During presentation of happy facial expressions, we detected a signal increase predominantly in the left anterior cingulate gyrus, bilateral posterior cingulate gyri, medial frontal cortex and right supramarginal gyrus, brain regions previously implicated in visuospatial and emotion processing tasks. No brain regions showed increased signal intensity during presentation of sad facial expressions. These results provide evidence for a distinction between the neural correlates of facial recognition memory and perception of facial expression but, whilst highlighting the role of limbic structures in perception of happy facial expressions, do not allow the mapping of a distinct neural substrate for perception of sad facial expressions.

Adult↗

Recall and recognition memory in amnesia: patients with hippocampal, medial temporal, temporal lobe or frontal pathology.

The relationship between recall and recognition memory impairments was examined in memory-disordered patients with either hippocampal, medial temporal, more widespread temporal lobe or frontal pathology. The Hirst [Hirst, W., Johnson, M. K., Phelps, E. A., & Volpe, B. T. (1988). More on recognition and recall in amnesics. Journal of Experimental Psychology: Learning, Memory, & Cognition, 14, 758-762] technique for titrating exposure times was used to match recognition memory performance as closely as possible before comparing recall memory scores. Data were available from two different control groups given differing exposure times. Each of the patient groups showed poorer recall memory performance than recognition scores, proportionate to the difference seen in healthy participants. When patients' scores were converted to Z-scores, there was no significant difference between mean Z-recall and Z-recognition scores. When plotted on a scatterplot, the majority of the data-points indicating disproportionately low recall memory scores came from healthy controls or patients with pathology extending into the lateral temporal lobes, rather than from patients with pathology confined to the medial temporal lobes. Patients with atrophy extending into the parahippocampal gyrus (H+) performed worse than patients with atrophy confined to the hippocampi (H-); but, when H- patients were given a shorter exposure time (5s) and compared with H+ at a longer exposure (10s), their performance was virtually identical and did not indicate any disproportionate recall memory impairment in the H- group. Parahippocampal volumes on MRI correlated significantly with both recall and recognition memory. The possibility that findings were confounded by inter-stimulus artefacts was examined and rejected. These findings argue against the view that hippocampal amnesia or memory disorders in general are typically characterised by a disproportionate impairment in recall memory. Disproportionate recall memory impairment has been observed in a number of published cases, and the reason for the varying pattern obtained across hippocampal patients requires further examination.

Adult↗

Visual recognition memory in specific learning-disabled children.

BACKGROUND: Reading depends on the efficient storage and retrieval of visual and verbal information. Some studies have shown deficits of specific learning-disabled children in the recall and recognition of visual stimuli. This deficit is usually interpreted to be secondary to a verbal labelling deficiency. In this experiment, we presented serial lists of complex geometric stimuli to a group of specific learning-disabled children (LD) and a non-disabled control group (NLD) at both the elementary and secondary school levels. We hypothesized that the NLD visual recognition performance would be superior to that of the LD group at the elementary school level, but not at the secondary school level. We further hypothesized that the difference was related to inefficient primary visual rehearsal strategies. METHODS: 20 elementary school children (11 LD and 9 NLD) and 31 secondary school children (15 LD and 16 NLD) were presented serial lists of four geometric figures. A probe was presented after a 1 second delay. The subjects pressed a key if the probe was in the list ("same" response) or another key if the probe was not in the list ("different" response). Type of response (correct or incorrect) and reaction time was measured at each serial position for "same" and "different" responses. RESULTS: At the elementary school level, there was a significant visual recognition memory advantage of the NLD group over the LD group (F(1,8) = 6.83, p = 0.018), but there was no significant difference between these groups at the secondary school level. There was no significant difference in the reaction time between the groups at either of the two levels. CONCLUSIONS: LD children have poorer visual recognition memory performance than NLD children for complex geometric patterns. Since there was no difference in reaction time between the two groups, attentional or encoding deficits can not adequately explain the recognition memory differences. The results can best be explained by inefficient visual rehearsal strategies with a small pool of visual items that are unfamiliar and difficult to code verbally. The serial recognition task can be used effectively by the optometrist to discriminate the performance of LD and NLD children.

Child↗

Changes in facial recognition memory across the adult life span.

We found significant and similar associations of facial recognition memory performance with age using two different methodologies: signal detection (SD) and delayed nonmatching-to-sample (DNM). These data demonstrate that previously reported associations between age and facial recognition memory performance were not specific to method of assessment, and that significant declines are seen as early as 50 years of age.

Adolescent↗

Excitotoxic lesions of the rhinal cortex in the baboon differentially affect visual recognition memory, habit memory and spatial executive functions.

To specify the functional role of the rhinal cortex, baboons with bilateral excitotoxic lesions of the rhinal cortex (RH group) were tested on a series of computerized memory and learning tasks. Preoperatively, they were trained to and then tested on a delayed nonmatching-to-sample (DNMS) task with trial-unique stimuli. Postoperatively, this visual recognition memory task was given twice. As compared to a sham-operated group, the RH group showed good retention of rule learning and were unimpaired on the Delay memory subtest. Performance on the List Length memory subtest was, however, severely impaired at both postoperative evaluations, with a significant negative correlation between cognitive performance and neuronal loss in rhinal areas. Visual habit memory and spatial working memory were assessed postoperatively only, using a concurrent discrimination learning task and both a delayed-response task (with a two- and four-location choice) and a delayed alternation task, respectively. The RH group was unimpaired on the first two tasks and was even faster than the controls in learning the delayed-response task with four locations. Finally, most RH baboons failed to learn the delayed alternation task within the limits of testing. These results indicate that neuronal loss in the rhinal cortex is sufficient to impair visual recognition memory, and extend the implication of this area to spatial executive functions. Furthermore, the observation of impaired recognition memory and executive processes with preserved procedural memory and retrograde memory suggests that damage to the rhinal cortex probably participates in the cognitive deficits typical of the early stages of Alzheimer's disease.

Animals↗

Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats.

Ischemia-induced cell loss in the CA1 region of the dorsal hippocampus results in severe deficits on delayed non-matching-to-sample (DNMS), whereas hippocampectomy produces little or no impairment, suggesting that partial hippocampal damage is more detrimental to DNMS performance than total ablation. To test this hypothesis, rats with or without preoperative DNMS training were given partial cytotoxic lesions of the dorsal hippocampus. When tested, neither group displayed any DNMS deficits despite widespread cell loss in the CA1 and other regions of the dorsal hippocampus. In the final experiments, rats tested previously on DNMS were found to be impaired on the Morris water maze. The finding that partial hippocampal lesions disrupt spatial memory while leaving object-recognition memory intact indicates a specialized role for the hippocampus in mnemonic processes.

Amnesia↗

Effects of sleep deprivation on short-term recognition memory.

A probe-recognition short-term memory paradigm was used to inquire into the precise effects of sleep deprivation on human memory. It was found that recognition performance, as measured by d', was generally impaired for each subjects after 24 hr of sleep deprivation. While d' was shown to decrease exponentially as the number of items intervening between the target and the probe increased, this decay rate was not affected by sleep loss. In addition there was confirmation of a previously observed increase in the positive skewness of reaction times after wakefulness. The data were consistent with the hypothesis that sleep deprivation increases the occurrence of lapses, periods of lowered reactive capacity, which prevent the encoding of items in short-term memory.

Adult↗

Iron deficiency alters auditory recognition memory in newborn infants of diabetic mothers.

Infants of diabetic mothers (IDMs) are at risk for perinatal brain iron deficiency that may target the developing hippocampus. The objective of this study was to evaluate hippocampally based recognition memory and infant development in IDMs with suspected brain iron deficiency (BID; cord ferritin </=34 microg/L) compared with IDMs with sufficient brain iron stores (BIS; cord ferritin >34 microg/L) using event-related potentials (ERPs). ERPs assessed neonatal auditory cortical responses to sounds and auditory recognition memory in response to the mother's voice compared with a stranger's voice. Thirty-two newborn IDMs had cord serum ferritin concentrations and provided neonatal ERP data (n = 23) and/or blinded 1 y developmental assessments (n = 28). Auditory cortical responses to speech and nonspeech sounds were similar in the BID and BIS groups. In the maternal voice recognition paradigm, peak latencies were shorter in the BID group than in the BIS group. Infants in the BIS group displayed a significant negative slow wave for the strangers' voices compared with the mothers' voices, whereas the BID group did not. Higher cord ferritin concentrations were correlated with larger negative slow waves at the right temporal (T4) electrode site. At 1 y of age, motor development was slower in the BID group than in the BIS group. IDMs suspected to have BID demonstrated impaired neonatal auditory recognition memory and lower psychomotor developmental scores at 1 y of age than IDMs with BIS. These impairments map onto areas of the developing brain known to be vulnerable to iron deficiency.

Auditory Perception↗

Recognition memory and introspective remember/know judgments: evidence for the influence of distractor plausibility on "remembering" and a caution about purportedly nonparametric measures.

One popular technique in the study of human recognition memory involves the elicitation of remember and know judgments and the attribution of those judgments to qualitative states of memory retrieval. An alternative view, reviewed here, implicates quantitative, but not qualitative, differences in evidence as the basis for those two judgments. That theory makes two clear and testable predictions: that of criterion shifts in "remembering" and that of isodiscriminability across different response sets. In this experiment, the makeup of the distractor set in a recognition test is shown to influence overall recognition criterion and also rates of "remember" responses. The second portion of the article demonstrates how A' is a poor choice of a measure to test the prediction of isodiscriminability. When this measure is corrected (Equation 7) to make it more consistent with current knowledge about the receiver-operating characteristic in recognition memory, it reveals that there is no difference in discriminability between "remember" and all positive responses.

Cognition↗

One process is not enough! A speed-accuracy tradeoff study of recognition memory.

Speed-accuracy tradeoff (SAT) methods have been used to contrast single- and dual-process accounts of recognition memory. In these procedures, subjects are presented with individual test items and are required to make recognition decisions under various time constraints. In this experiment, we presented word lists under incidental learning conditions, varying the modality of presentation and level of processing. At test, we manipulated the interval between each visually presented test item and a response signal, thus controlling the amount of time available to retrieve target information. Study-test modality match had a beneficial effect on recognition accuracy at short response-signal delays (< or =300 msec). Conversely, recognition accuracy benefited more from deep than from shallow processing at study only at relatively long response-signal delays (> or =300 msec). The results are congruent with views suggesting that both fast familiarity and slower recollection processes contribute to recognition memory.

Auditory Perception↗

Reversal of age-related deficits in object recognition memory in rats with l-deprenyl.

The monoamine-oxidase-B (MAO-B) inhibitor l-deprenyl (selegiline) is effective in treating Parkinson's disease and possibly cognitive deficits associated with aging, Alzheimer's disease and HIV dementia. The aim of the present study was to investigate the effects of l-deprenyl on short- and long-term recognition memory in aged rats. Young adult and aged male Wistar rats were trained in a novel object recognition task. Retention test trials were carried out at 1.5 or 24 h after training. Aged rats showed impaired recognition memory retention 24 h after training when compared to young animals. Treatment with a daily systemic injection of l-deprenyl (1.0 mg/kg) for 21 days reversed the memory impairment. A control experiment indicated that l-deprenyl did not affect sensorimotor functions. The results suggest that l-deprenyl reverses age-related deficits in long-term recognition memory.

Aging↗

The development of recognition memory for the left-right orientation of pictures.

3 studies examined the development of recognition memory for the left-right orientation of pictures of common objects. In study 1, 5-year-olds, 9-year-olds, and college students were shown 20 pictures of objects. Subsequently, they were tested on their ability to discriminate between 10 of these pictures and their left-right mirror images and between the other 10 pictures and completely new ones. There were large developmental differences in memory for orientation, although all age groups could discriminate accurately between familiar pictures and completely new ones. In studies 2a and 2b, training concerning the relevance of orientation improved second and fourth graders' long-term memory for this characteristic, but training effects were minimal for kindergartners. However, even kindergarten children showed accurate short-term memory for orientation on the task used for training. In contrast to study 2, study 3 produced accurate long-term memory for orientation in kindergarten children by using a verbal training procedure. Results are discussed in terms of the range of memory factors involved in children's mirror-image confusions and in terms of general implications for the development of recognition memory.

Adolescent↗

Recognition memory for single tones with and without context.

Sequences of seven tones were presented, and recognition memory for individual tones of each sequence was tested under varying degrees of context. With no context, the test required recognition of a tone isolated from the sequence; with full context, the tone to be recognized was embedded in the original sequence. A series of three experiments demonstrated that recognition memory was far more accurate under full-context conditions than under no-context conditions and that the superiority was not wholly attributable to the serial position information or the order information provided by the full context. It is suggested that in addition to the processing of limited information for the pitch of isolated tones, pattern (or relational) information is abstracted from a tone sequence and is retrieved in the presence of full context.

Association↗

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.

Adult↗

Continuous recognition memory tests: are the assumptions of the theory of signal detection met?

Two continuous recognition memory tests were administered to 20 males and 20 females using the confidence rating procedure to determine if the underlying assumptions of the theory of signal detection (TSD) are met by these tasks. Z-score transformed ROC curves proved to be straight lines parallel to the positive diagonal of the ROC graph. These findings suggest that the distributions of familiarity for old and new stimuli are normal and of equal variance for the Continuous Recognition Memory and Continuous Visual Memory Tests. TSD interpretation of test data appears to be justified.

Adolescent↗

Signal-detection, threshold, and dual-process models of recognition memory: ROCs and conscious recollection.

Threshold- and signal-detection-based models have dominated theorizing about recognition memory. Building upon these theoretical frameworks, we have argued for a dual-process model in which conscious recollection (a threshold process) and familiarity (a signal-detection process) contribute to memory performance. In the current paper we assessed several memory models by examining the effects of levels of processing and the number of presentations on recognition memory receiver operating characteristics (ROCs). In general, when the ROCs were plotted in probability space they exhibited an inverted U shape; however, when they were plotted in z space they exhibited a U shape. An examination of the ROCs showed that the dual-process model could account for the observed ROCs, but that models based solely on either threshold or signal-detection processes failed to provide a sufficient account of the data. Furthermore, an examination of subjects' introspective reports using the remember/know procedure showed that subjects were aware of recollection and familiarity and were able to consistently report on their occurrence. The remember/know data were used to accurately predict the shapes of the ROCs, and estimates of recollection and familiarity derived from the ROC data mirrored the subjective reports of these processes.

Adult↗