Brain areas interconnected to ventral pathway circuits are independently able to induce enhancement in object recognition memory and cause reversal in object recognition memory deficit.

AIMS: Ventral pathway circuits are constituted by the interconnected brain areas that are distributed throughout the brain. These brain circuits are primarily involved in processing of object related information in brain. However, their role in object recognition memory (ORM) enhancement remains unknown. Here, we have studied on the implication of these circuits in ORM enhancement and in reversal of ORM deficit in aging. METHODS: The brain areas interconnected to ventral pathway circuits in rat brain were activated by an expression of a protein called regulator of G-protein signaling 14 of 414 amino acids (RGS14414). RGS14414 is an ORM enhancer and therefore used here as a gain-in-function tool. ORM test and immunohistochemistry, lesions, neuronal arborization, and knockdown studies were performed to uncover the novel function of ventral pathway circuits. RESULTS: An activation of each of the brain areas interconnected to ventral pathway circuits individually induced enhancement in ORM; however, same treatment in brain areas not interconnected to ventral pathway circuits produced no effect. Further study in perirhinal cortex (PRh), area V2 of visual cortex and frontal cortex (FrC), which are brain areas that have been shown to be involved in ORM and are interconnected to ventral pathway circuits, revealed that ORM enhancement seen after the activation of any one of the three brain areas was unaffected by the lesions in other two brain areas either individually in each area or even concurrently in both areas. This ORM enhancement in all three brain areas was associated to increase in structural plasticity of pyramidal neurons where more than 2-fold higher dendritic spines were observed. Additionally, we found that an activation of either PRh, area V2, or FrC not only was adequate but also was sufficient for the reversal of ORM deficit in aging rats, and the blockade of RGS14414 activity led to loss in increase in dendritic spine density and failure in reversal of ORM deficit. CONCLUSIONS: These results suggest that brain areas interconnected to ventral pathway circuits facilitate ORM enhancement by an increase in synaptic connectivity between the local brain area circuits and the passing by ventral pathway circuits and an upregulation in activity of ventral pathway circuits. In addition, the finding of the reversal of ORM deficit through activation of an interconnected brain area might serve as a platform for developing not only therapy against memory deficits but also strategies for other brain diseases in which neuronal circuits are compromised.

Identification of Early Hippocampal Dynamics during Recognition Memory with Independent Component Analysis.

The hippocampus is generally considered to have relatively late involvement in recognition memory, its main electrophysiological signature being between 400 and 800 ms after stimulus onset. However, most electrophysiological studies have analyzed the hippocampus as a single responsive area, selecting only a single-site signal exhibiting the strongest effect in terms of amplitude. These classical approaches may not capture all the dynamics of this structure, hindering the contribution of other hippocampal sources that are not located in the vicinity of the selected site. We combined intracerebral electroencephalogram recordings from epileptic patients with independent component analysis during a recognition memory task involving the recognition of old and new images. We identified two sources with different responses emerging from the hippocampus: a fast one (maximal amplitude at ∼250 ms) that could not be directly identified from raw recordings and a latter one, peaking at ∼400 ms. The former component presented different amplitudes between old and new items in 6 out of 10 patients. The latter component had different delays for each condition, with a faster activation (∼290 ms after stimulus onset) for recognized items. We hypothesize that both sources represent two steps of hippocampal recognition memory, the faster reflecting the input from other structures and the latter the hippocampal internal processing. Recognized images evoking early activations would facilitate neural computation in the hippocampus, accelerating memory retrieval of complementary information. Overall, our results suggest that the hippocampal activity is composed of several sources with an early activation related to recognition memory.

Age-Differential Role of Gaze Reinstatement in Recognition Memory for Negative Visual Stimuli.

OBJECTIVES: Although research has shown that the replay of encoding-specific gaze patterns during retrieval, known as gaze reinstatement, facilitates memory retrieval, little is known about whether it differentially associates with the negativity preference in memory (defined as enhanced memory for negative stimuli relative to neutral stimuli in this study) among younger and older adults. The present study aims to address this research gap. METHODS: A total of 33 older adults (16 women; aged 58-69 years, M = 63.48, SD = 2.98) and 36 younger adults (10 women; aged 18-26 years, M = 20.39, SD = 1.57) completed a remember/know recognition memory task involving negative and neutral pictures. Their eye movements were tracked during both the memory encoding and retrieval phases. RESULTS: Younger and older adults had better memory for negative than neutral pictures. Older adults exhibited significantly stronger gaze reinstatement for negative than neutral stimuli, while this difference was nonsignificant in younger adults. Moreover, gaze reinstatement is positively linked to memory performance in both age groups. DISCUSSION: The results suggest that gaze reinstatement may play age-differential roles in the negativity preference of memory. Negative valence may enhance gaze reinstatement, which improves subsequent recognition memory, particularly among older adults. The finding contributes to a better understanding of the mechanisms underlying the negative preference for memory in different age groups.

Tuned geometries of hippocampal representations meet the computational demands of social memory.

Social memory consists of two processes: the detection of familiar compared with novel conspecifics and the detailed recollection of past social episodes. We investigated the neural bases for these processes using calcium imaging of dorsal CA2 hippocampal pyramidal neurons, known to be important for social memory, during social/spatial encounters with novel conspecifics and familiar littermates. Whereas novel individuals were represented in a low-dimensional geometry that allows for generalization of social identity across different spatial locations and of location across different identities, littermates were represented in a higher-dimensional geometry that supports high-capacity memory storage. Moreover, familiarity was represented in an abstract format, independent of individual identity. The degree to which familiarity increased the dimensionality of CA2 representations for individual mice predicted their performance in a social novelty recognition memory test. Thus, by tuning the geometry of structured neural activity, CA2 is able to meet the demands of distinct social memory processes.

Neural correlates of impaired learning and recognition of novel faces in mild cognitive impairment.

OBJECTIVE: Face memory impairment significantly affects social interactions and daily functioning in individuals with mild cognitive impairment (MCI). While deficits in recognizing familiar faces among individuals with MCI have been reported, their ability to learn and recognize unfamiliar faces remains unclear. This study examined the behavioral performance and event-related potentials (ERPs) of unfamiliar face memorization and recognition in MCI. METHODS: Fifteen individuals with MCI and 15 healthy controls learned and recognized 90 unfamiliar neutral faces. Their performance accuracy and cortical ERPs were compared between the two groups across the learning and recognition phases. RESULTS: Individuals with MCI had lower accuracy in identifying newly learned faces than healthy controls. Moreover, individuals with MCI had reduced occipitotemporal N170 and central vertex positive potential responses during both the learning and recognition phases, suggesting impaired initial face processing and attentional resources allocation. Also, individuals with MCI had reduced central N200 and frontal P300 responses during the recognition phase, suggesting impaired later-stage face recognition and attention engagement. CONCLUSION: These findings provide neurobehavioral evidence for impaired learning and recognition of unfamiliar faces in individuals with MCI. SIGNIFICANCE: Individuals with MCI may have face memory deficits in both early-stage face processing and later-stage recognition .

Catcalls: exotic cats discriminate the voices of familiar caregivers.

Background: The ability to differentiate familiar from unfamiliar humans has been considered a product of domestication or early experience. Few studies have focused on voice recognition in Felidae despite the fact that this family presents the rare opportunity to compare domesticated species to their wild counterparts and to examine the role of human rearing. Methods: We tested whether non-domesticated Felidae species recognized familiar human voices by exposing them to audio playbacks of familiar and unfamiliar humans. In a pilot study, we presented seven cats of five species with playbacks of voices that varied in familiarity and use of the cats' names. In the main study, we presented 24 cats of 10 species with unfamiliar and then familiar voice playbacks using a habituation-dishabituation paradigm. We anticipated that human rearing and use of the cats' names would result in greater attention to the voices, as measured by the latency, intensity, and duration of responses regardless of subject sex and subfamily. Results: Cats responded more quickly and with greater intensity (e.g., full versus partial head turn, both ears moved versus one ear twitching) to the most familiar voice in both studies. They also responded for longer durations to the familiar voice compared to the unfamiliar voices in the main study. Use of the cats' name and rearing history did not significantly impact responding. These findings suggest that close human contact rather than domestication is associated with the ability to discriminate between human voices and that less social species may have socio-cognitive abilities akin to those of more gregarious species. With cats of all species being commonly housed in human care, it is important to know that they differentiate familiar from unfamiliar human voices.

Comparison with others influences encoding and recognition of their faces: Behavioural and ERP evidence.

In daily life, faces are often memorized within contexts involving interpersonal interactions. However, little is known about whether interpersonal interaction-related contexts influence face memory. The present study aimed to understand this question by investigating how social comparison-related context affects face encoding and recognition. To address this issue, 40 participants were informed that they and another player each played a monetary game and were then presented with both of their outcomes (either monetary gain or loss). Subsequently, participants were shown the face of the player whom they were just paired with. After all the faces had been encoded, participants were asked to perform a sudden old/new recognition task involving these faces. The results showed that, during the encoding phase, another player's monetary gain, compared to loss, resulted in more negative responses in the N170 and early posterior negativity (EPN)/N250 to relevant players' faces when participants encountered monetary loss and a smaller late positive potential (LPP) response irrespective of self-related outcomes. In the subsequent recognition phase, preceding another player's monetary gain as compared to loss led to better recognition performance and stronger EPN/N250 and LPP responses to the faces of relevant players when participants had lost some amount of money. These findings suggest that the social comparison-related context, particularly self-disadvantageous outcomes in the context, influences the memory of comparators' faces.

No verbal overshadowing in aphantasia: The role of visual imagery for the verbal overshadowing effect.

The verbal overshadowing effect refers to the phenomenon that the verbal description of a past complex stimulus impairs its subsequent recognition. Theoretical explanations range from interference between different mental representations to the activation of different processing orientations or a provoked shift in the recognition criterion. In our study, 61 participants with aphantasia (= lack of mental imagery) and 70 controls participated in a verbal overshadowing paradigm. The verbal overshadowing effect did not occur in people with aphantasia, although the effect was replicated in controls. We speculate that this is either due to the lack of visual representations in people with aphantasia that verbal descriptions could interfere with, or to the absence of a shift in processing orientation during verbalisation. To rule out criterion-based explanations, further research is needed to distinguish between discriminability and response bias in people with aphantasia. Finally, data indicated that the verbal overshadowing effect may even be reversed in individuals with aphantasia, partly due to a lower memory performance in the no verbalisation condition. Effects of further variables are discussed, such as mental strategies, memory confidence, and difficulty, quantity and quality of verbalisation.

A role of frontal association cortex in long-term object recognition memory of objects with complex features in rats.

Perirhinal cortex is a brain area that has been considered crucial for the object recognition memory (ORM). However, with the use of an ORM enhancer named RGS14414 as gain-in-function tool, we show here that frontal association cortex and not the Perirhinal cortex is essential for the ORM of objects with complex features that consisted of detailed drawing on the object surface (complex ORM). An expression of RGS14414, in rat brain frontal association cortex, induced the formation of long-term complex ORM, whereas the expression of the same memory enhancer in Perirhinal cortex failed to produce this effect. Instead, RGS14414 expression in Perirhinal cortex caused the formation of ORM of objects with simple features that consisted of the shape of object (simple ORM). Further, a selective elimination of frontal association cortex neurons by treatment with an immunotoxin Ox7-SAP completely abrogated the formation of complex ORM. Thus, our results suggest that frontal association cortex plays a key role in processing of a high-order recognition memory information in brain.

Encoding-related Brain Activity Predicts Subsequent Trial-level Control of Proactive Interference in Working Memory.

Proactive interference (PI) appears when familiar information interferes with newly acquired information and is a major cause of forgetting in working memory. It has been proposed that encoding of item-context associations might help mitigate familiarity-based PI. Here, we investigate whether encoding-related brain activation could predict subsequent level of PI at retrieval using trial-specific parametric modulation. Participants were scanned with event-related fMRI while performing a 2-back working memory task with embedded 3-back lures designed to induce PI. We found that the ability to control interference in working memory was modulated by level of activation in the left inferior frontal gyrus, left hippocampus, and bilateral caudate nucleus during encoding. These results provide insight to the processes underlying control of PI in working memory and suggest that encoding of temporal context details support subsequent interference control.

BDNF-dependent signaling in the olfactory bulb modulates social recognition memory in mice.

An operative olfactory bulb (OB) is critical to social recognition memory (SRM) in rodents, which involves identifying conspecifics. Furthermore, OB also allocates synaptic plasticity events related to olfactory memories in their intricate neural circuit. Here, we asked whether the OB is a target for brain-derived neurotrophic factor (BDNF), a well-known mediator of plasticity and memory. Adult ICR-CD1 male mice had their SRM evaluated under the inhibition of BDNF-dependent signaling directly in the OB. We also quantified the expression of BDNF in the OB, after SRM acquisition. Our results presented an amnesic effect of anti-BDNF administered 12 h post-training. Although the western blot showed no statistical difference in pro-BDNF and BDNF expression, the analysis of fluorescence intensity in slices suggests SRM acquisition decreases BDNF in the granular cell layer of the OB. Next, to test the ability of BDNF to rescue SRM deficit, we administered the human recombinant BDNF (rBDNF) directly in the OB of socially isolated (SI) mice. Unexpectedly, rBDNF did not rescue SRM in SI mice. Furthermore, BDNF and pro-BDNF expression in the OB was unchanged by SI. Our study reinforces the OB as a plasticity locus in memory-related events. It also adds SRM as another type of memory sensitive to BDNF-dependent signaling.

Can mirror self-recognition in mice unpack the neural underpinnings of self-awareness?

In this issue of Neuron, Yokose et al. show that mice groom a mark on their forehead when exposed to a mirror. Comparing this behavior with hominids' helps carve self-awareness into its component parts and explore the neural mechanisms of its shared components.

The beneficial effects of concept definition and interactive imagery tasks on associative memory: Evidence from event-related potentials.

It is widely accepted that familiarity can support associative memory when the to-be-remember items are unitized into a new representation. However, there has been relatively little attention devoted to investigating the effects of different unitization manipulations on associative memory. The present study aimed to address this gap by examining the effects of varying levels of unitization through three tasks: Concept definition, interactive imagery, and sentence frame tasks. The behavioral results revealed that associative memory was significantly enhanced in the interactive imagery task compared to the sentence frame task. However, no significant differences were found between the sentence frame and concept definition tasks, or between the concept definition and interactive imagery tasks. In terms of the neural correlates, the event-related potential (ERP) results revealed that the sentence frame task only elicited a significant recollection-related LPC old/new effect, while the concept definition task only elicited a significant familiarity-related FN400 old/new effect. However, the interactive representation task elicited both of these distinct effects. These findings suggest that both the concept definition and interactive imagery tasks can enhance familiarity for supporting associative memory, but their beneficial effects on associative memory or LPC old/new effects may be different.

The effect of chronic academic stress on intentional forgetting.

This study investigated whether chronic academic stress could affect the directed forgetting (DF) process. Both the stress group (undergoing preparation for a major academic examination) and the control group performed a DF task. A forgetting cue was presented after a to-be-forgotten (TBF) word, whereas no cue appeared after a to-be-remembered (TBR) item in the study phase. An old/new recognition test was used in the test phase. The results showed that (1) the stress group showed a higher level of self-reported stress, state anxiety, negative affect, and decreased cortisol awakening response (CAR) compared with the control group, suggesting a higher level of stress for the stress group. (2) Both groups showed superior recognition performance of TBR than TBF items, suggesting a DF effect. (3) The stress group showed inferior recognition performance of TBF items and an enhanced DF effect compared with the control group. These results demonstrated that the intentional memory control process might be enhanced under chronic academic stress.

Using transcranial direct current stimulation (tDCS) to selectively modulate the face inversion effect and N170 event-related potentials.

We report a large study (n = 72) using combined transcranial direct current stimulation-electroencephalography (tDCS-EEG) to investigate the modulation of perceptual learning indexed by the face inversion effect. Participants were engaged with an old/new recognition task involving intermixed upright and inverted, normal and Thatcherized faces. The accuracy results showed anodal tDCS delivered at the Fp3 scalp area (cathode/reference electrode placed at Fp2) increased the behavioural inversion effect for normal faces versus sham/control and this covaried with a modulation of the N170 event-related potential component. A reduced inversion effect for normal faces was found on the N170 latency and amplitude versus sham/control, extending recent work that combined tDCS and EEG in circumstances where the behavioural face inversion effect was reduced. Our results advance understanding of the neural mechanisms responsible for perceptual learning by revealing a dissociation between the N170 amplitude and latency in response to the tDCS-induced modulation of the face inversion effect. The behavioural modulation of the inversion effect tracks the modulation of the N170 amplitudes, albeit it is negatively correlated (i.e., reduced inversion effect-larger N170 amplitude inversion effect, increased inversion effect-reduced N170 amplitude inversion effect). For the N170 latencies, the inversion effect is reduced by the tDCS protocol we use irrespective of any modulation of the behavioural inversion effect.

The generality of the attentional boost effect for famous, unfamiliar, and inverted faces.

Familiarity and face inversion not only affect face recognition and memory but also influence attention. Face processing is less attention-demanding for familiar than for unfamiliar faces and for upright than for inverted faces. The automaticity raises the question of how face processing interacts with an increase in attention. Using a dual-task paradigm, we tested the interaction between attention and face familiarity and orientation. Participants encoded a series of faces to memory while simultaneously monitoring a stream of colored squares, pressing the space bar for target-colored squares and making no response to distractor-colored squares. Replicating previous findings of the attentional boost effect (ABE), we found that faces encoded with target squares were better remembered than faces encoded with distractor squares. If the automatic nature of familiar (or upright) face processing makes attention unnecessary, then the attentional boost should be attenuated for familiar relative to unfamiliar faces and for upright relative to inverted faces. Data from three experiments showed, however, that the ABE was the same for all types of faces. These results suggest that target detection did not simply elevate attention in an early encoding phase. Rather, selecting targets and rejecting distractors in the color task may have led to yoked temporal selection of target-concurrent faces for entry into memory.

Assessing partial errors via analog gaming keyboards in response conflict tasks: A proof-of-concept study with the concealed information test.

The response time-based Concealed Information Test (RT-CIT) is an established memory detection paradigm. Slower RTs to critical information (called 'probes') compared to control items (called 'irrelevants') reveal recognition. Different lines of research indicate that response conflict is a strong contributor to this RT difference. Previous studies used electromyography (EMG) to measure response conflict, but this requires special equipment and trained examiners. The aim of this study was to explore if response conflict can also be measured with an analog gaming keyboard that is sensitive to minimal finger movements. In a preregistered study, participants completed an autobiographical RT-CIT (n = 35) as well as a cued recognition task (modified Sternberg task; n = 33) for validation purposes. Partial errors, partial button presses of the incorrect response key, were more frequent in trials with response conflict than in trials without conflict. Partial errors were rare (CIT: 2.9%; Sternberg: 1.7% of conflict trials), suggesting analogue keyboards have lower sensitivity than EMG. This is the first evidence that analog keyboards can measure partial errors. Although likely less sensitive than EMG measures, potential benefits of analog keyboards include their accessibility, their compatibility with all tasks that use a standard keyboard, that no physical contact with the participant is needed, and ease of data collection (e.g., allowing for group testing).

Does context recollection depend on the base-rate of contextual features?

Episodic recollection is defined by the re-experiencing of contextual and target details of a past event. The base-rate dependency hypothesis assumes that the retrieval of one contextual feature from an integrated episodic trace cues the retrieval of another associated feature, and that the more often a particular configuration of features occurs, the more effective this mutual cueing will be. Alternatively, the conditional probability of one feature given another feature may be neglected in memory for contextual features since they are not directly bound to one another. Three conjoint recognition experiments investigated whether memory for context is sensitive to the base-rates of features. Participants studied frequent versus infrequent configurations of features and, during the test, they were asked to recognise one of these features with (vs. without) another feature reinstated. The results showed that the context recollection parameter, representing the re-experience of contextual features in the dual-recollection model, was higher for frequent than infrequent feature configurations only when the binding of feature information was made easier and the differences in the base-rates were extreme, otherwise no difference was found. Similarly, base-rates of features influenced response guessing only in the condition with salient differences in base-rates. The Bayes factor analyses showed that the evidence from two of our experiments favoured the base-rate neglect hypothesis over the base-rate dependency hypothesis; the opposite result was obtained in the third experiment, but only when high base-rate disproportion and facilitated feature binding conditions were used.

Differential effects of intrinsic properties of natural scenes and interference mechanisms on recognition processes in long-term visual memory.

Humans display remarkable long-term visual memory (LTVM) processes. Even though images may be intrinsically memorable, the fidelity of their visual representations, and consequently the likelihood of successfully retrieving them, hinges on their similarity when concurrently held in LTVM. In this debate, it is still unclear whether intrinsic features of images (perceptual and semantic) may be mediated by mechanisms of interference generated at encoding, or during retrieval, and how these factors impinge on recognition processes. In the current study, participants (32) studied a stream of 120 natural scenes from 8 semantic categories, which varied in frequencies (4, 8, 16 or 32 exemplars per category) to generate different levels of category interference, in preparation for a recognition test. Then they were asked to indicate which of two images, presented side by side (i.e. two-alternative forced-choice), they remembered. The two images belonged to the same semantic category but varied in their perceptual similarity (similar or dissimilar). Participants also expressed their confidence (sure/not sure) about their recognition response, enabling us to tap into their metacognitive efficacy (meta-d'). Additionally, we extracted the activation of perceptual and semantic features in images (i.e. their informational richness) through deep neural network modelling and examined their impact on recognition processes. Corroborating previous literature, we found that category interference and perceptual similarity negatively impact recognition processes, as well as response times and metacognitive efficacy. Moreover, images semantically rich were less likely remembered, an effect that trumped a positive memorability boost coming from perceptual information. Critically, we did not observe any significant interaction between intrinsic features of images and interference generated either at encoding or during retrieval. All in all, our study calls for a more integrative understanding of the representational dynamics during encoding and recognition enabling us to form, maintain and access visual information.

The role of recollection, familiarity, and the hippocampus in episodic and working memory.

The hippocampus plays an essential role in long-term episodic memory by supporting the recollection of contextual details, whereas surrounding regions such as the perirhinal cortex support familiarity-based recognition discriminations. Working memory - the ability to maintain information over very brief periods of time - is traditionally thought to rely heavily on frontoparietal attention networks, but recent work has shown that it can also rely on the hippocampus. However, the conditions in which the hippocampus becomes involved in working memory tasks are unclear and whether it contributes to recollection or familiarity-based responses in working memory is only beginning to be explored. In the current paper, we first review and contrast the existing amnesia literature examining recollection and familiarity in episodic and working memory. The results indicate that recollection and familiarity contribute to both episodic and working memory. However, in contrast to episodic memory, in working memory the hippocampus is particularly critical for familiarity-based rather than recollection-based discrimination. Moreover, the results indicate that the role of the hippocampus in working memory can be obscured due to 'criterion-induced process-masking' because it primarily supports intermediate-confidence recognition decisions. We then report results from a new working memory study examining the ability of amnesics to detect global and local changes in novel complex objects (i.e., fribbles), which indicates that the hippocampus plays an especially critical role in working memory when the task requires the detection of global rather than discrete changes. We conclude by considering the results in light of neurocomputational models and proposing a general framework for understanding the relationship between episodic and working memory.