Human Recognition Memory Research Articles

Recognition memory signals in the macaque hippocampus

The hippocampus plays a critical role in recognition memory in both monkeys and humans. However, neurophysiological studies have rarely reported recognition memory signals among hippocampal neurons. The majority of these previous studies used variants of the delayed match-to-sample task; however, studies of the effects of hippocampal damage in monkey and humans have shown that another task of recognition memory, the visual paired-comparison, or visual preferential looking task (VPLT), is more sensitive to hippocampal damage than the delayed matching tasks. Accordingly, to examine possible recognition memory signals in the hippocampus, we recorded the activity of 131 hippocampal neurons in two monkeys performing the VPLT. Eighty-eight neurons (67%) responded significantly to stimulus presentation relative to the baseline prestimulus period. A substantial proportion of these visually responsive neurons (36%) showed significant firing-rate modulations that reflected whether stimuli were novel or familiar. Additionally, these firing-rate modulations were correlated with recognition memory performance on the VPLT such that larger modulations by stimulus novelty were associated with better performance. Together, these results provide evidence for a neural signal in the hippocampus that may support recognition memory performance.

Reward Motivation Accelerates the Onset of Neural Novelty Signals in Humans to 85 Milliseconds

SummaryThe neural responses that distinguish novel from familiar items in recognition memory tasks are remarkably fast in both humans and nonhuman primates. In humans, the earliest onsets of neural novelty effects emerge at about ∼150–200 ms after stimulus onset [1–5]. However, in recognition memory studies with nonhuman primates, novelty effects can arise at as early as 70–80 ms [6, 7]. Here, we address the possibility that this large species difference in onset latencies is caused experimentally by the necessity of using reward reinforcement to motivate the detection of novel or familiar items in nonhuman primates but not in humans. Via magnetoencephalography in humans, we show in two experiments that the onset of neural novelty signals is accelerated from ∼200 ms to ∼85 ms if correct recognition memory for either novel or familiar items is rewarded. Importantly, this acceleration is independent of whether the detection of the novel or the familiar scenes is rewarded. Furthermore, this early novelty effect contributed to memory retrieval because neural reward responses, which were contingent upon novelty detection, followed ∼100 ms later. Thus, under the contextual influence of reward motivation, behaviorally relevant novelty signals emerge much faster than previously held possible in humans.

Recognition Memory, Familiarity, and Déjà vu Experiences

Déjà vu occurs when one feels as though a situation is familiar, despite evidence that the situation could not have been experienced before. Until recently, the topic of déjà vu remained largely outside of the realm of mainstream scientific investigation. However, interest in investigating the nature of déjà vu is growing among researchers of cognitive processes. In some cases, déjà vu may be understood within the context of research on human recognition memory. Specifically, déjà vu may sometimes result from familiarity-based recognition, or recognition that is based on feelings of familiarity that occur without identification of their source.

Selective attention in human associative learning and recognition memory.

Four experiments examined the role of selective attention in a new causal judgment task that allowed measurement of both causal strength and cue recognition. In Experiments 1 and 2, blocking was observed; pretraining with 1 cue (A) resulted in reduced learning about a 2nd cue (B) when those 2 cues were trained in compound (AB+). Participants also demonstrated decreased recognition performance for the causally redundant Cue B, suggesting that less attention had been paid to it in training. This is consistent with the idea that attention is preferentially allocated toward the more predictive Cue A, and away from the less predictive Cue B (e.g., N. J. Mackintosh, 1975). Contrary to this hypothesis, in Experiments 3 and 4, participants demonstrated poorer recognition for the most predictive cues, relative to control cues. A new model, which is based on N. J. Mackintosh's (1975) model, is proposed to account for the observed relationship between the extent to which each cue is attended to, learned about, and later recognized

Computational models can replicate the capacity of human recognition memory

The capacity of human recognition memory was investigated by Standing, who presented several groups of participants with different numbers of pictures (from 20 to 10 000), and subsequently tested their ability to distinguish between previously presented and novel pictures. The estimated number of pictures retained in recognition memory by different groups when plotted as a logarithmic function of the number of pictures presented formed a straight line, representing a power–law relationship. Here, we investigate if published models of familiarity discrimination can replicate Standing's results. We first consider a simplified assumption that visual stimuli are represented by uncorrelated patterns of firing of visual neurons providing input to the familiarity discrimination network. We show that for this case three models (Familiarity discrimination based on Energy (FamE), Anti-Hebbian and Info-max) can reproduce the observed power–law relationship when their synaptic weights are appropriately initialized. For more realistic assumptions on neural representation of stimuli, the FamE model is no longer able to reproduce the power–law relationship in simulations, while the Anti-Hebbian and Info-max can reproduce it. Nevertheless, the slopes of the power–law relationships produced by the models in all simulations differ from that observed by Standing. We discuss possible reasons for this difference, including separate contributions of familiarity and recollection processes, and describe experimentally testable predictions based on our analysis.

Course of relational and non-relational recognition memory across the adult lifespan

Human recognition memory shows a decline during normal ageing, which is thought to be related to age-associated dysfunctions of mediotemporal lobe structures. Whether the hippocampus is critical for human general relational memory or for spatial relational memory only is still disputed. The human perirhinal cortex is thought to be critically involved in non-relational memory, but another view postulates hippocampal involvement in both relational and non-relational memory. Investigating whether there is a differential impact of ageing on these memory processes may shed further light into these issues. Thus, in the present study, 106 healthy adults performed three recognition memory tasks in a consecutive age groups design involving a range from age 20 to 76. This allowed the separate assessment of spatial and nonspatial relational memory as well as non-relational memory. Both spatial and nonspatial relational memory declined in the 66-76 yr group. This pattern is consistent with the presumed course of hippocampal changes across normal ageing and points to the hippocampal role in relational memory in general. An impairment of non-relational memory commenced earlier in the 51-65 yr group. This finding is discussed in relation to perceptual/attentional mediation of memory and its potential brain correlates in ageing.

Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations.

The perirhinal cortex (PRh) is widely accepted as having an important role in object recognition memory in humans and animals. Contrary to claims that PRh mediates declarative memory exclusively, previous evidence suggests that PRh has a role in the perceptual processing of complex objects. In the present study, we conducted an examination of the possible role of PRh in perceptual function in rats. We examined whether bilateral excitotoxic lesions of PRh or PPRh (perirhinal plus postrhinal cortices) in the rat would cause deficits in a zero-delay object-recognition task and a simultaneous oddity discrimination task. Both of these tasks measured spontaneous (untrained, unrewarded) behavior, and the stimuli in these experiments were manipulated to produce varying levels of perceptual difficulty. As predicted by simulations using a computational model, rats with PPRh lesions were impaired in object recognition when the stimuli to be discriminated were manipulated to share many features in common. Furthermore, rats with PPRh and PRh lesions were impaired in a simultaneous oddity discrimination task when the stimuli to be discriminated were manipulated explicitly to be more perceptually similar. These findings provide support for the idea that PRh in the rat is important for the perceptual processing of complex objects, in addition to its well established role in memory.

Effects of sex on object recognition and spatial navigation in humans

Human tests designed to mirror rodent tests of object recognition and spatial navigation were administered to adult cognitively healthy humans. Facial recognition was also assessed. There was no sex difference in facial recognition, consistent with earlier studies. In the object recognition test, the test–retest NINL total scores during the same visit were highly correlated, comparable to the test–retest correlations obtained in the established facial recognition test. There were no effects of sex on object recognition. However, in the spatial navigation test, there were effects of sex on spatial learning and memory during the session with the hidden, but not visible, target. These tests might be useful to compare assessments of object recognition and spatial learning and memory in humans and animal models.

Memory Strength and Repetition Suppression: Multimodal Imaging of Medial Temporal Cortical Contributions to Recognition

Declarative memory permits an organism to recognize stimuli that have been previously encountered, discriminating them from those that are novel. One basis for recognition is item memory strength, which may support the perception of stimulus familiarity. Though the medial temporal lobes are known to be critical for declarative memory, at present the neural mechanisms supporting perceived differences in memory strength remain poorly specified. Here, functional MRI (fMRI) and anatomically constrained magnetoencephalography (MEG) indexed correlates of graded memory strength in the human brain, focusing on medial temporal cortex. fMRI revealed a decrease in medial temporal cortical activation that tracked parametric levels of perceived memory strength. Anatomically constrained MEG current estimates revealed that strength-dependent signal reductions onset within 150-300 ms. Memory strength appears to be rapidly signaled by medial temporal cortex through repetition suppression (activation reductions), providing a basis for the subjective perception of stimulus familiarity or novelty.

Evidence that baroreflex feedback influences long-term incidental visual memory in men

Sympathetic nervous system (SNS) activity at the time of acquisition is associated with human memory. However, rather than SNS activity per se, it may be afferent baroreflex feedback that is responsible for this effect. A pharmacological design was employed to unload (SNP, sodium nitro-prusside) and load (norepinephrine) baroreceptors. In addition to two placebo periods, epinephrine and esmolol (a peripherally acting β1-blocker) served as control conditions for altered cardiac perception. During drug infusion blood pressure, heart rate, and perception of heartbeat were tested. Twenty-four healthy men were participated. The participants viewed emotional slides while their electromyographic eye blink responses to random noise bursts were measured (affective startle modulation paradigm) to determine potential drug impact on emotional processing. Subjects were not informed that memory testing would take place after 4 weeks. Drugs did not impact startle, thus indicating unbiased emotional processing at the time of acquisition. Norepinephrine had no effect on heartbeat perception, but improved ( p = .002) recognition memory. SNP ( p = .0001) increased heartbeat perception but impaired ( p = .038) recognition memory. Epinephrine, on the other hand, increased heartbeat perception ( p = .0001) yet did not impair but partially improve memory (effect on high arousing pictures only: p = .05). Heartbeat perception in the placebo condition did not correlate with recognition memory ( p’s > .5). We suggest that baroreflex unloading, with subsequent feedback activation of the SNS, impairs long-term incidental visual recognition memory in humans while baroreflex loading enhances it. Further, we propose that these memory effects are neither secondary to cardiac sensations that accompany SNS activation nor to altered emotional picture processing at the time of acquisition.

A Mini-Review of fMRI Studies of Human Medial Temporal Lobe Activity Associated with Recognition Memory

This review considers event-related functional magnetic resonance imaging (fMRI) studies of human recognition memory that have or have not reported activations within the medial temporal lobes (MTL). For comparisons both between items at study (encoding) and between items at test (recognition), MTL activations are characterized as left/right, anterior/posterior, and hippocampus/surrounding cortex, and as a function of the stimulus material and relevance of item/source information. Though no clear pattern emerges, there are trends suggesting differences between item and source information, and verbal and spatial information, and a role for encoding processes during recognition tests. Important future directions are considered.

Magnetoencephalographic correlates of different levels in subjective recognition memory

In our current study we employed whole-head magnetoencephalography (MEG) to identify neurophysiological correlates (event-related fields, ERFs) of different phenomenologies in human recognition memory. Words which had previously been semantically processed were presented along with previously unstudied words. Via button presses, participants provided subjective indices of three forms of memory: confident recognition, familiarity-based recognition, and misclassification of previously presented items as new (no recognition, misses). Behavioral results revealed a clear distinction between confident recognition (shortest reaction times) and familiarity-based recognition and misses, respectively, and physiological data pointed to bilateral anterior and left anterior/central regions in which magnetic field patterns were directly related to word recognition from ∼300 ms to 500 ms after word onset. In the context of the prevalent dual process controversy on the roles of familiarity and recollection in recognition memory, we first highlight that two operationalizations of recollection need to be differentiated: We argue that a strategic search for a particular contextual feature stands in clear contrast to the fast and incidental availability of some contextual feature and derive experimental and behavioral indicators for either form of recollection. These indicators are used to select from manifold cognitive neuroscientific work on recognition memory in order to further discuss the neurocognitive characteristics of incidental recollection in contrast to other forms of episodic memory.

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.

Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory.

Damage to perirhinal cortex (PRh) impairs object recognition memory in humans, monkeys, and rats when tested in tasks such as delayed nonmatching to sample, visual paired comparison, and its rodent analog, the spontaneous object recognition task. In the present study, we have capitalized on the discrete one-trial nature of the spontaneous object recognition task to investigate the role of PRh in several distinct stages of object recognition memory. In a series of experiments, transient inactivation of PRh was accomplished with bilateral infusions of lidocaine directly into PRh immediately before the sample phase (encoding), immediately before the choice phase (retrieval), or within the retention delay after the sample phase (storage-consolidation). Compared with performance on trials in which they received saline infusions, rats were significantly impaired when lidocaine was infused before the sample phase, regardless of the length of the retention delay. Similarly, delay-independent deficits were observed after immediate pre-choice infusions of lidocaine. Finally, PRh inactivation immediately and 20 min after the sample phase, but not 40, 60, or 80 min after, also disrupted subsequent object recognition when the retention delay was sufficiently long to ensure the dissipation of the actions of lidocaine during the choice phase. The effects of pre-sample and pre-choice inactivation indicate involvement of PRh in encoding and retrieval stages of object recognition, and the time course of post-sample inactivation effects suggests a role for PRh in the maintenance of the object trace during memory consolidation.

Acetylcholine, histamine, and cognition: two sides of the same coin.

The forebrain cholinergic neurons are localized in the nucleus basalis magnocellularis (NBM), the major source of cholinergic innervation to the neocortex and to the amygdala, and in the medium septum-banda diagonalis complex, which provides cholinergic inputs to the hippocampus (Mesulam et al. 1983; Woolf et al. 1984; Nicoll 1985). Basic and clinical studies have linked dysfunctions of these neurons to cognitive decline (Everitt and Robbins 1997; Givens and Sarter 1997). Their extensive loss is characteristic of the forebrain of Alzheimer’s disease patients (Davies and Maloney 1976; Coyle et al. 1983; Kuhl et al. 1999), and anticholinergic drugs, such as scopolamine and atropine, produce learning and memory deficits in a variety of cognitive animal models (Deutsch 1971; Bartus and Johnson 1976; Ennaceur and Meliani 1992), and affect recognition memory in humans (Sperling et al. 2002; Sherman et al. 2003). Moreover, aged rodents display both cognitive impairments in many learning tasks (Ingram et al. 1994) and cholinergic deficits (Kubanis and Zornetzer 1981; Decker 1987; Gallagher and Colombo 1995). However, neuronal alterations associated with cognitive deficits are not restricted to the cholinergic systems. For instance, dysfunctions of dopamine, GABA, noradrenaline, serotonin, and histamine neurons have been identified in Alzheimer’s disease (Hardy et al. 1985; Airaksinen et al. 1991; Panula et al. 1997; Schneider et al. 1997), and region-selective decreases in dopaminergic, noradrenergic, or serotonergic contents are associated with the level of age-related learning and memory impairments (Stemmelin et al. 2000; Birthelmer et al. 2003). Abnormal interactions between malfunctioning cholinergic and other neurotransmitter systems may cause additive or even synergistic effects on cognition, a phenomenon that warrants the increasing interest in understanding the complex physiology of brain systems affecting cognitive processes. In this regard, the role of histamine is gaining increasing attention (Passani et al. 2000; Passani and Blandina 2003), and many recent results indicate that the histaminergic system influences learning and memory by modulating the release of ACh (Passani et al. 2000; Bacciottini et al. 2001), although some cognitive effects of histamine and histaminergic agents occur independently of ACh. For example, local administration of histamine failed to affect ACh release from the hippocampus (Bacciottini et al. 2002), yet improved fear memory by H2or H3-receptor-elicited erk2 activation in hippocampal CA3 cells (Giovannini et al. 2003). Nevertheless, histaminergic efferents influence both the NBM-cortical (Clapham and Kilpatrick 1992; Blandina et al. 1996; Cecchi et al. 2001) and the medium septum-banda diagonalis-hippocampal cholinergic pathways (Mochizuki et al. 1994; Bacciottini et al. 2002; Fig. 1). The regulation of ACh tone in different brain areas by neuronal histamine also encompasses functions other than cognition. Histamine promotes wakefulness by tonic control over sleep-generating mechanisms in the preoptic/anterior hypothalamus, and cholinergic neurons seem to be implicated (Lin et al. 1994; Brown et al. 2001). The aim of this review is to summarize some of the most recent work on the interactions between histaminergic and cholinergic systems, and evaluate their role in cognitive and other brain functions.

Human Hippocampal and Parahippocampal Activity during Visual Associative Recognition Memory for Spatial and Nonspatial Stimulus Configurations

Evidence from animal studies points to the importance of the parahippocampal region (PHR) [including entorhinal, perirhinal, and parahippocampal (PHC) cortices] for recognition of visual stimuli. Recent findings in animals suggest that PHR may also be involved in visual associative recognition memory for configurations of stimuli. Thus far, however, such involvement has not been demonstrated in humans. In fact, it has been argued that associative recognition in humans is critically dependent on the hippocampal formation (HF). To better understand the division of function between HF and PHR during recognition memory in humans, we measured the activity of both areas in healthy young adults during an associative recognition memory task using functional magnetic resonance imaging. To more precisely characterize the nature of the associations that might be coded by the HF and PHR during recognition, subjects were required to learn and were later tested for associations based on either the spatial arrangements of two stimuli or the identity of two stimuli (a face and a tool). An area in the PHC was found to be more active for recognized old configurations than new configurations in both the spatial and identity conditions. The HF, on the other hand, was more active for recognition of new configurations than old configurations and also more active in the spatial than the identity condition. These data highlight the involvement of PHR in the long-term coding of associative relationships between stimuli and help to clarify the nature of its functional distinction from the HF.

Prefrontal cortex contribution to associative recognition memory in humans: an event-related functional magnetic resonance imaging study

The present event-related fMRI study examined in ten healthy participants neural correlates of recognition memory for intact, rearranged, and new pairs of visual stimuli. The correct categorization of both intact and rearranged pairs relative to pairs of new, never presented before stimuli relies on the retrieval of associative information whereas the discrimination of rearranged pairs from intact pairs additionally involves a recall-to-reject process by which subjects retrieve additional information to reach a recognition decision. Relative to new pairs, both intact and rearranged pairs yielded activation in inferior prefrontal cortex bilaterally and left dorsolateral prefrontal cortex. Relative to intact pairs, rearranged pairs were associated with increased activity in left dorsolateral prefrontal cortex. The latter could reflect the neural correlates of a recall-to-reject process, a pivotal process of associative recognition memory.

Functional connectivity of gamma EEG activity is modulated at low frequency during conscious recollection

We examined two subjectively distinct memory states that are elicited during recognition memory in humans and compared them in terms of the gamma oscillations (20–60 Hz) in the electroencepahalogram (EEG) that they induced. These subjective states, ‘ recollection’ and ‘ familiarity’ both entail correct recognition but one involves a clear and conscious recollection of the event including memory for contextual detail whilst the other involves a sense of familiarity without clear recollection. Here we show that during a verbal recognition memory test, the subjective experience of ‘ recollection’ induced higher amplitude gamma oscillations than the subjective experience of ‘ familiarity’ in the time period 300–500 ms after stimulus presentation. Recollection, but not familiarity, was also associated with greater functional connectivity in the gamma frequency range between frontal and parietal sites. Furthermore, the magnitude of the gamma functional connectivity varied over time and was modulated at 3 Hz. Previous studies in animals have shown local theta frequency modulation (3–7 Hz) of gamma-oscillations but this is the first time that a similar effect has been reported in the human EEG.

Cognitive theories as reinforcement history surrogates: the case of likelihood ratio models of human recognition memory.

B. F. Skinner (1977) once argued that cognitive theories are essentially surrogates for the organism's (usually unknown) reinforcement history. In this article, we argue that this notion applies rather directly to a class of likelihood ratio models of human recognition memory. The point is not that such models are fundamentally flawed or that they are not useful and should be abandoned. Instead, the point is that the role of reinforcement history in shaping memory decisions could help to explain what otherwise must be explained by assuming that subjects are inexplicably endowed with the relevant distributional information and computational abilities. To the degree that a role for an organism's reinforcement history is appreciated, the importance of animal memory research in understanding human memory comes into clearer focus. As Skinner was also fond of pointing out, it is only in the animal laboratory that an organism's history of reinforcement can be precisely controlled and its effects on behavior clearly understood.

Dissociating familiarity from recollection in human recognition memory: different rates of forgetting over short retention intervals.

Two functionally distinct forms of recognition memory have been identified in human and nonhuman species-the ability to recollect qualitative information about previous events, and the ability to differentiate between familiar and novel stimuli. Separate dual-process theories have been developed in the animal and human literatures to account for these findings. However, it is not clear whether these theories describe the same two underlying memory processes. On the basis of animal studies of medial temporal lobe function, familiarity is expected to exhibit disproportionately fast forgetting compared with recollection over short retention intervals. We tested this prediction in healthy human subjects by examining recognition forgetting rates across a range of 8-32 intervening items and found significant forgetting in the accuracy of familiarity-based discriminations and no evidence of forgetting in the accuracy of recollection-based discriminations. In agreement with the results from nonhuman species, the present results indicate that item familiarity decreases more rapidly than recollection over short retention intervals.