Recency Discrimination Research Articles

Temporal memory for threatening events encoded in a haunted house

ABSTRACT Despite the salient experience of encoding threatening events, these memories are prone to distortions and often non-veridical from encoding to recall. Further, threat has been shown to preferentially disrupt the binding of event details and enhance goal-relevant information. While extensive work has characterised distinctive features of emotional memory, research has not fully explored the influence threat has on temporal memory, a process putatively supported by the binding of event details into a temporal context. Two primary competing hypotheses have been proposed; that threat can impair or enhance temporal memory. We analysed two datasets to assess temporal memory for an in-person haunted house experience. In study 1, we examined the temporal structure of memory by characterising memory contiguity in free recall as a function of individual levels of heart rate as a proxy of threat. In study 2, we replicated marginal findings of threat-related increases in memory contiguity found in study 1. We extended these findings by showing threat-related increases in recency discriminations, an explicit test of temporal memory. Together, these findings demonstrate that threat enhances temporal memory regarding free recall structure and during explicit memory judgments.

Cortical reorganization of the glutamate synapse in the activity-based anorexia rat model: Impact on cognition.

Patients suffering from anorexia nervosa (AN) display altered neural activity, morphological, and functional connectivity in the fronto‐striatal circuit. In addition, hypoglutamatergic transmission and aberrant excitability of the medial prefrontal cortex (mPFC) observed in AN patients might underpin cognitive deficits that fuel the vicious cycle of dieting behavior. To provide a molecular mechanism, we employed the activity‐based anorexia (ABA) rat model, which combines the two hallmarks of AN (i.e., caloric restriction and intense physical exercise), to evaluate structural remodeling together with alterations in the glutamatergic signaling in the mPFC and their impact on temporal memory, as measured by the temporal order object recognition (TOOR) test. Our data indicate that the combination of caloric restriction and intense physical exercise altered the homeostasis of the glutamate synapse and reduced spine density in the mPFC. These events, paralleled by an impairment in recency discrimination in the TOOR test, are associated with the ABA endophenotype. Of note, after a 7‐day recovery period, body weight was recovered and the mPFC structure normalized but ABA rats still exhibited reduced post‐synaptic stability of AMPA and NMDA glutamate receptors associated with cognitive dysfunction. Taken together, these data suggest that the combination of reduced food intake and hyperactivity affects the homeostasis of the excitatory synapse in the mPFC contributing to maintain the aberrant behaviors observed in AN patients. Our findings, by identifying novel potential targets of AN, may contribute to more effectively direct the therapeutic interventions to ameliorate, at least, the cognitive effects of this psychopathology.

Distributed interactive brain circuits for object-in-place memory: A place for time?

Rodents will spontaneously learn the location of an individual object, an ability captured by the object-in-place test. This review considers the network of structures supporting this behavioural test, as well as some potential confounds that may affect interpretation. A hierarchical approach is adopted, as we first consider those brain regions necessary for two simpler, ‘precursor’ tests (object recognition and object location). It is evident that performing the object-in-place test requires an array of areas additional to those required for object recognition or object location. These additional areas include the rodent medial prefrontal cortex and two thalamic nuclei (nucleus reuniens and the medial dorsal nucleus), both densely interconnected with prefrontal areas. Consequently, despite the need for object and location information to be integrated for the object-in-place test, for example, via the hippocampus, other contributions are necessary. These contributions stem from how object-in-place is a test of associative recognition, as none of the individual elements in the test phase are novel. Parallels between the structures required for object-in-place and for recency discriminations, along with a re-examination of the demands of the object-in-place test, signal the integration of temporal information within what is usually regarded as a spatial-object test.

Infection Staging and Incidence Surveillance Applications of High Dynamic Range Diagnostic Immuno-Assay Platforms

Custom HIV staging assays, including the Sedia HIV-1 Limiting Antigen (LAg) Avidity EIA and avidity modifications of the Ortho VITROS anti-HIV-1+2 and Abbott ARCHITECT HIV Ag/Ab Combo assays, are used to identify "recent" infections in clinical settings and for cross-sectional HIV incidence estimation. However, the high dynamic range of chemiluminescent platforms allows differentiating recent and long-standing infection on signal intensity, and this raises the prospect of using unmodified diagnostic assays for infection timing and surveillance applications. We tested a panel of 2500 well-characterized specimens with estimable duration of HIV infection with the 3 assays and the unmodified ARCHITECT. Regression models were used to estimate mean durations of recent infection (MDRIs), context-specific false-recent rates (FRRs) and correlation between diagnostic signal intensity and LAg measurements. Hypothetical epidemiological scenarios were constructed to evaluate utility in surveillance applications. Over a range of MDRIs (reflecting recency discrimination thresholds), a diluted ARCHITECT-based RITA produced lower FRRs than the VITROS platform (FRR ≈ 0.5% and 1.5%, respectively at MDRI ≈ 200 days), and the unmodified diagnostic ARCHITECT produces incidence estimates with comparable precision to LAg (relative SE ≈ 17.5% and 15%, respectively at MDRI ≈ 200 days). ARCHITECT S/CO measurements were highly correlated with LAg optical density measurements (r = 0.80), and values below 200 are strongly predictive of LAg recency and duration of infection less than 1 year. Low quantitative measurements from the unmodified ARCHITECT obviate the need for additional recency testing, and its use is feasible in clinical staging and incidence surveillance applications.

The retrosplenial cortex and object recency memory in the rat.

It has been proposed that the retrosplenial cortex forms part of a ‘where/when’ information network. The present study focussed on the related issue of whether retrosplenial cortex also contributes to ‘what/when’ information, by examining object recency memory. In Experiment 1, rats with retrosplenial lesions were found to be impaired at distinguishing the temporal order of objects presented in a continuous series (‘Within‐Block’ condition). The same lesioned rats could, however, distinguish between objects that had been previously presented in one of two discrete blocks (‘Between‐Block’ condition). Experiment 2 used intact rats to map the expression of the immediate‐early gene c‐fos in retrosplenial cortex following performance of a between‐block, recency discrimination. Recency performance correlated positively with levels of c‐fos expression in both granular and dysgranular retrosplenial cortex (areas 29 and 30). Expression of c‐fos in the granular retrosplenial cortex also correlated with prelimbic cortex and ventral subiculum c‐fos activity, the latter also correlating with recency memory performance. The combined findings from both experiments reveal an involvement of the retrosplenial cortex in temporal order memory, which includes both between‐block and within‐block problems. The current findings also suggest that the rat retrosplenial cortex comprises one of a group of closely interlinked regions that enable recency memory, including the hippocampal formation, medial diencephalon and medial frontal cortex. In view of the well‐established importance of the retrosplenial cortex for spatial learning, the findings support the notion that, with its frontal and hippocampal connections, retrosplenial cortex has a key role for both what/when and where/when information.

Temporal memory is shaped by encoding stability and intervening item reactivation.

Making sense of previous experience requires remembering the order in which events unfolded in time. Prior work has implicated the hippocampus and medial temporal lobe cortex in memory for temporal information associated with individual episodes. However, the processes involved in encoding and retrieving temporal information across extended sequences is relatively poorly understood. Here we used fMRI during the encoding and retrieval of extended sequences to test specific predictions about the type of information used to resolve temporal order and the role of the hippocampus in this process. Participants studied sequences of images of celebrity faces and common objects followed by a recency discrimination test. The main conditions of interest were pairs of items that had been presented with three intervening items, half of which included an intervening category shift. During encoding, hippocampal pattern similarity across intervening items was associated with subsequent successful order memory. To test for evidence of associative retrieval, we trained a classifier to discriminate encoding patterns associated with faces versus objects and applied the classifier on fMRI patterns during recency discrimination. We found evidence that the category content of intervening items was reactivated during recency judgments, and this was related to hippocampal encoding-retrieval similarity. A follow-up behavioral priming experiment revealed additional evidence for intervening item reinstatement during temporal order judgments. Reinstatement did not differ according to whether the items occurred within a single context or across context boundaries. Thus, these data suggest that inter-item associative encoding and retrieval mediated by the hippocampus contribute to temporal order memory.

Contrasting networks for recognition memory and recency memory revealed by immediate-early gene imaging in the rat.

The expression of the immediate-early gene c-fos was used to compare networks of activity associated with recency memory (temporal order memory) and recognition memory. In Experiment 1, rats were first familiarized with sets of objects and then given pairs of different, familiar objects to explore. For the recency test group, each object in a pair was separated by 110 min in the time between their previous presentations. For the recency control test, each object in a pair was separated by less than a 1 min between their prior presentations. Temporal discrimination of the objects correlated with c-fos activity in the recency test group in several sites, including area Te2, the perirhinal cortex, lateral entorhinal cortex, as well as the dentate gyrus, hippocampal fields CA3 and CA1. For both the test and control conditions, network models were derived using structural equation modeling. The recency test model emphasized serial connections from the perirhinal cortex to lateral entorhinal cortex and then to the CA1 subfield. The recency control condition involved more parallel pathways, but again highlighted CA1 within the hippocampus. Both models contrasted with those derived from tests of object recognition (Experiment 2), because stimulus novelty was associated with pathways from the perirhinal cortex to lateral entorhinal cortex that then involved both the dentate gyrus (and CA3) and CA1 in parallel. The present findings implicate CA1 for the processing of familiar stimuli, including recency discriminations, while the dentate gyrus and CA3 pathways are recruited when the perirhinal cortex signals novel stimuli.

Dissociation of recognition and recency memory judgments after anterior thalamic nuclei lesions in rats.

The anterior thalamic nuclei form part of a network for episodic memory in humans. The importance of these nuclei for recognition and recency judgments remains, however, unclear. Rats with anterior thalamic nuclei lesions and their controls were tested on object recognition, along with two types of recency judgment. The spontaneous discrimination of a novel object or a novel odor from a familiar counterpart (recognition memory) was not affected by anterior thalamic lesions when tested after retention delays of 1 and 60 min. To measure recency memory, rats were shown two familiar objects, one of which had been explored more recently. In one condition, rats were presented with two lists (List A, List B) of objects separated by a delay, thereby creating two distinct blocks of stimuli. After an additional delay, rats were presented with pairs of objects, one from List A and one from List B (between-block recency). No lesion-induced deficit was apparent for recency discriminations between objects from different lists, despite using three different levels of task difficulty. In contrast, rats with anterior thalamic lesions were significantly impaired when presented with a continuous list of objects and then tested on their ability to distinguish between those items early and late in the same list (within-block recency). The contrasting effects on recognition and recency support the notion that interlinked hippocampal–anterior thalamic interconnections support aspects of both spatial and nonspatial learning, although the role of the anterior thalamic nuclei may be restricted to a subclass of recency judgments (within-block).

Temporal Memory Dysfunction and Alterations in Tyrosine Hydroxylase Immunoreactivity in Adult Rats Following Neonatal Exposure to Domoic Acid

The purpose of the present study was to determine whether early alterations in glutamate signaling, via daily injections of the glutamate agonist, domoic acid (DOM; 20 μg/kg), during a critical period of CNS development (PND 8 - 14), would result in temporal memory deficits and/or alterations in tyrosine hydroxylase (TH) immunoreactivity. As adults, subjects were assessed for temporal memory ability using a recency discrimination paradigm. Both number and duration of exploratory contacts directed at familiar objects, differing by one hour in recall delay, were measured. Analyses revealed that DOM-treated females demonstrated temporal memory dysfunction, as evidenced in a significantly lower proportion of total exploratory behaviour directed toward the remote object. Integrity of the dopamine system was assessed using immunohistochemistry to examine TH immunoreactivity in the prefrontal cortex (PFC) and nucleus accumbens (NAcc). Sections obtained from DOM-treated males had significantly less TH immunoreactivity in the right mPFC, while DOM-treated females had significantly greater TH immunoreactivity in the left core and right shell of the NAcc. These findings are discussed in context of early alterations to glutamate signaling in the development of human neuropsychiatric disorders.

The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition

In humans recognition memory deficits, a typical feature of diencephalic amnesia, have been tentatively linked to mediodorsal thalamic nucleus (MD) damage. Animal studies have occasionally investigated the role of the MD in single-item recognition, but have not systematically analyzed its involvement in other recognition memory processes. In Experiment 1 rats with bilateral excitotoxic lesions in the MD or the medial prefrontal cortex (mPFC) were tested in tasks that assessed single-item recognition (novel object preference), associative recognition memory (object-in-place), and recency discrimination (recency memory task). Experiment 2 examined the functional importance of the interactions between the MD and mPFC using disconnection techniques. Unilateral excitotoxic lesions were placed in both the MD and the mPFC in either the same (MD + mPFC Ipsi) or opposite hemispheres (MD + mPFC Contra group). Bilateral lesions in the MD or mPFC impaired object-in-place and recency memory tasks, but had no effect on novel object preference. In Experiment 2 the MD + mPFC Contra group was significantly impaired in the object-in-place and recency memory tasks compared with the MD + mPFC Ipsi group, but novel object preference was intact. Thus, connections between the MD and mPFC are critical for recognition memory when the discriminations involve associative or recency information. However, the rodent MD is not necessary for single-item recognition memory.

A Specific Role of the Human Hippocampus in Recall of Temporal Sequences

There is a growing interest in how temporal order of episodic memories is represented within the medial temporal lobe (MTL). Animal studies suggest that the hippocampal formation (HF) is critical for retrieving the temporal order of past experiences. However, human imaging studies that have tested recency discrimination between pairs of previously encoded items have generally failed to report HF activation. We hypothesized that recalling a naturalistic sequence of past events would be particularly sensitive to HF function, attributable to greater involvement of associative processes. To test this prediction, we let subjects watch a novel movie and later, during functional magnetic resonance imaging, asked them to rearrange and "replay" scenes from the movie in correct order. To identify areas specifically involved in retrieval of temporal order, we used a control condition where subjects logically inferred the order of scenes from the same movie. Extensive MTL activation was observed during sequence recall. Activation within the right HF was specifically related to retrieval of temporal order and correlated positively with accuracy of sequence recall. Also, the bilateral parahippocampal cortex responded to retrieval of temporal order, but the activation here was not related to performance. Our study is the first to unequivocally demonstrate that correct sequence recall depends on HF.

The relationship of recency discrimination to explicit memory and executive functioning

Recency discrimination has been conceptualized as an executive ability by some investigators and as an aspect of episodic memory by others. We compared the performance of 261 neurologically healthy adults on a recency discrimination task (RDT) with their performance on measures of executive functioning and explicit memory. Mean z-transformed raw scores were used to construct indices of visual and verbal explicit memory, fluency, and executive functioning. Analyses revealed that RDT performance correlated more closely with visual (r = 0.32; p < 0.001) and verbal memory (r = 0.25; p < 0.001) than with fluency (r = 0.16; p < 0.05) and executive functioning (r = 0.13; p < 0.05). These findings suggest that recency discrimination might be better understood as an aspect of episodic memory that is subserved primarily by hippocampal and medial temporal structures than as an executive function that is subserved primarily by prefrontal cortex.

Recognition Memory for Objects, Place, and Temporal Order: A Disconnection Analysis of the Role of the Medial Prefrontal Cortex and Perirhinal Cortex

Recognition memory requires judgments of the previous occurrence of stimuli made on the basis of the relative familiarity of individual objects, or by integrating information concerning objects and location, or by using recency information. The present study examined the role of the medial prefrontal cortex (mPFC) and perirhinal cortex (PRH) in these distinct recognition memory processes using a series of behavioral tests: a novel object preference task, an object-in-place task, and a temporal order memory task. Also, a disconnection procedure was used to test whether these regions form components of an integrated system for recognition memory. Male DA rats received bilateral lesions in the PRH or mPFC or unilateral lesions placed in both cortices in either the same (PRH-mPFC IPSI) or contralateral (PRH-mPFC CONTRA) hemispheres. A fifth group underwent sham surgery (SHAM). In the object-in-place and temporal order memory tasks, the PRH, mPFC, and PRH-mPFC CONTRA groups were significantly impaired. However, performance in the novel object preference task was only impaired in the PRH group. No group was impaired in the object location task. These results demonstrate that the mPFC and PRH are crucial for object-in-place associational and recency discriminations, whereas the PRH but not the mPFC is important for the discrimination of novel and familiar individual objects. Importantly, these results provide direct support for the hypothesis that to make discriminations based on associational or recency information, both cortical regions operate within an integrated neural network for recognition memory.

Interaction between perirhinal and medial prefrontal cortex is required for temporal order but not recognition memory for objects in rats.

The present study investigated the roles of the perirhinal cortex, medial prefrontal cortex, and intrahemispheric interactions between them in recognition and temporal order memory for objects. Experiment 1 assessed the effects of bilateral microinfusions of the sodium channel blocker lidocaine into either the anterior perirhinal or medial prefrontal cortex immediately before memory testing in a familiarity discrimination task and a recency discrimination task, both of which involved spontaneous exploration of objects. Inactivation of the perirhinal cortex disrupted performance in both tasks, whereas inactivation of the medial prefrontal cortex disrupted performance in the recency, but not the familiarity, discrimination task. In a second experiment, the importance of intrahemispheric interactions between these structures in temporal order memory were assessed by comparing the effects of unilateral inactivation of either structure alone with those of crossed unilateral inactivation of both structures on the recency discrimination task. Crossed unilateral inactivation of both structures produced a significant impairment, whereas inactivation of either structure alone produced little or no impairment. Collectively, these findings suggest that the perirhinal cortex, but not the medial prefrontal cortex, contributes to retrieval of information necessary for long-term object recognition, whereas both structures, via intrahemispheric interactions between them, contribute to retrieval of information necessary for long-term object temporal order memory. These data are consistent with models in which attributed information is stored in posterior cortical sites and supports lower-order mnemonic functions (e.g., recognition memory) but can also be retrieved and further processed via interactions with the prefrontal cortex to support higher-order mnemonic functions (e.g., temporal order memory).

ERP old/new effects at different retention intervals in recency discrimination tasks

Recognition memory studies have suggested that event-related brain potentials (ERPs) may tap into several different memory processes. In particular, two ERP components have been hypothesized as related to familiarity (FN400 old/new effect, 300–500 ms, anterior) and recollection processes (parietal old/new effect, 400–800 ms, posterior). The functional significance of the FN400 old/new effect is uncertain because similar old/new differences have been shown to disappear at moderately long retention intervals. The present study investigated the effects of retention interval (34 min, 39 min, or 1 day) on the FN400 and parietal old/new effects in two different recency discrimination tasks. The results suggest that the FN400 old/new effect can be maintained across 1-day retention intervals, so it may index brain processes capable of contributing to long-term memory.

Schizophrenia-like syndrome inducing agent phencyclidine failed to impair memory for temporal order in rats

Although subchronic phencyclidine (PCP) administration is recognized as a probative method to model schizophrenia-like symptoms in animals, only a few sets of data support the hypothesis of a cognitive prefrontal cortex (PFc) dysfunction in PCP-treated monkeys and rodents. Two experiments were here conducted to further test the integrity of prefrontal function in two versions of a memory for temporal order (MTO) task administered to rats. Original versions of this task elaborated by Kesner ( Chiba, Kesner, & Gibson, 1997; Chiba, Kesner, & Reynolds, 1994; Kesner & Holbrook, 1987) repeatedly yielded moderate to severe performance deficits in PFc lesioned rats. MTO assessment in an eight-arm radial maze consisted in a recency discrimination between two arms previously explored in the context of sequential forced choices. In Experiment 1, 16 naive Long-Evans rats were pre-trained on a variable version of the MTO task involving randomly re-mixed sequences until they reached a group criterion. Then, rats were treated daily for 21 days with PCP (10 mg/kg) or saline vehicle and were tested on the same task approximately 20 h after an injection. The performance of the groups did not differ. In Experiment 2, 16 naive Long-Evans rats untrained prior to treatment received 27 daily injections of either PCP (10 mg/kg) or saline vehicle and were tested, 20 h after each injection, on a constant version of the MTO task. This time, a fixed set of four sequences of successive arm entries was repeated within each daily session as well as across days. Again, prolonged PCP exposure failed to impair discrimination of temporal order despite the stability of sequential information over time. These negative results are not consistent with long-lasting hypofrontality, a major landmark of human schizophrenia, in the PCP rat model.

The role of the frontal lobes in memory: evidence from unilateral frontal resections for relief of intractable epilepsy

The current investigation explored processes associated with memory deficits in patients with frontal lobe dysfunction. Specifically, we examined deficits associated with the encoding, consolidation, and retrieval of information in memory in 53 patients who underwent either a unilateral frontal (N=13) or temporal (N=40) lobe resection for relief of intractable epilepsy. Post-surgical memory scores indicated that the frontal group and the temporal group did not differ in consolidation of information, as defined by the information forgotten between immediate and delayed recall. Instead, the temporal group evidenced significantly poorer recall of verbal information at both immediate and delayed recall. This effect was especially strong in the left temporal group for the recall of verbal information. Although no group differences were observed in the degree to which patients semantically organized information or made recency discriminations, the frontal group exhibited significantly weaker release from proactive interference than the temporal group, suggesting some impairment in encoding and retrieval processes associated with frontal lobe dysfunction.

The role of the frontal lobes in memory: evidence from unilateral frontal resections for relief of intractable epilepsy

The current investigation explored processes associated with memory deficits in patients with frontal lobe dysfunction. Specifically, we examined deficits associated with the encoding, consolidation, and retrieval of information in memory in 53 patients who underwent either a unilateral frontal (N=13) or temporal (N=40) lobe resection for relief of intractable epilepsy. Post-surgical memory scores indicated that the frontal group and the temporal group did not differ in consolidation of information, as defined by the information forgotten between immediate and delayed recall. Instead, the temporal group evidenced significantly poorer recall of verbal information at both immediate and delayed recall. This effect was especially strong in the left temporal group for the recall of verbal information. Although no group differences were observed in the degree to which patients semantically organized information or made recency discriminations, the frontal group exhibited significantly weaker release from proactive interference than the temporal group, suggesting some impairment in encoding and retrieval processes associated with frontal lobe dysfunction.

Modelling relative recency discrimination tasks using a stochastic working memory model

Relative recency discrimination (RD) task is typically used to assess the temporal organization function of the prefrontal cortex (PFC). Subjects look at a series of cards (with words or drawings on them) and on seeing a test card determine which of the two items was seen more recently. Results show that patients with damage to the prefrontal cortex are severely impaired on this task. We propose a memory trace-priming mechanism, based on automatic time-marking process hypothesis (Schacter, D.L., 1987. Memory, amnesia, and frontal lobe dysfunction: a critique and interpretation. Psychobiology 15, 21–36), to offer a computational account of the results. In this model, successive words seen by subjects leave decaying memory traces in PFC, which subsequently prime the representations in higher sensory areas such as inferior temporal Cortex (IT) during discrimination judgements. The paper focuses on the evaluation of a probabilistic pre-frontal trace mechanism using a pool of clusters of neurons with self-sustained firing that ends at a random time. The results show that the probabilistic behavior of subjects can be accounted for by the stochasticity of the trace model. A good fit to experimental data is obtained with a PFC memory persistence probability with a decay time constant of τ=∼30 s. The model allows for a distributed representation in IT and PFC, but the best fit suggests a sparse representation. It is concluded that further data are needed on representations in IT and PFC, on the connectivity between these two areas, and on the statistical and dynamic properties of memory neurons in PFC.

Differential involvement of the human temporal lobe structures in short- and long-term memory processes assessed by intracranial ERPs.

Intracranial event-related potentials (ERPs) elicited during a recognition memory task were recorded in 25 epileptic patients by using depth electrodes sampling four different regions within the temporal lobe (amygdala, hippocampus, anterior and posterior temporal cortices). The task was a continuous recognition memory task in which repeated items were presented after 6 or 19 intervening items following their first presentation. This study was performed to investigate the respective role of the different temporal lobe structures in short-term memory (STM) and long-term memory (LTM) processing. Subregions of the temporal lobe were differently involved in these two memory systems. The posterior temporal cortex is specifically involved in STM processing, whereas the amygdala, hippocampus, and anterior temporal cortex contribute to both STM and LTM. Moreover, it appeared that the latter structures play their own role in LTM. The anterior temporal cortex and amygdala may contribute to recency discrimination, and the hippocampus seems rather to be involved in maintaining memory traces. These findings suggest that the temporal lobe structures may function in a complementary way by subserving different aspects of information processing.