Shared neural codes of recognition memory.

Recognition memory research has identified several electrophysiological indicators of successful memory retrieval, known as old-new effects. These effects have been observed in different sensory domains using various stimulus types, but little attention has been given to their similarity or distinctiveness and the underlying processes they may share. Here, a data-driven approach was taken to investigate the temporal evolution of shared information content between different memory conditions using openly available EEG data from healthy human participants of both sexes, taken from six experiments. A test dataset involving personally highly familiar and unfamiliar faces was used. The results show that neural signals of recognition memory for face stimuli were highly generalized starting from around 200 ms following stimulus onset. When training was performed on non-face datasets, an early (around 200-300 ms) to late (post-400 ms) differentiation was observed over most regions of interest. Successful cross-classification for non-face stimuli (music and object/scene associations) was most pronounced in late period. Additionally, a striking dissociation was observed between familiar and remembered objects, with shared signals present only in the late window for correctly remembered objects, while cross-classification for familiar objects was successful in the early period as well. These findings suggest that late neural signals of memory retrieval generalize across sensory modalities and stimulus types, and the dissociation between familiar and remembered objects may provide insight into the underlying processes.

Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation.

Reorientation, the process of regaining one's bearings after becoming lost, requires identification of a spatial context (context recognition) and recovery of facing direction within that context (heading retrieval). We previously showed that these processes rely on the use of features and geometry, respectively. Here, we examine reorientation behavior in a task that creates contextual ambiguity over a long timescale to demonstrate that male mice learn to combine both featural and geometric cues to recover heading. At the neural level, most CA1 neurons persistently align to geometry, and this alignment predicts heading behavior. However, a small subset of cells remaps coherently in a context-sensitive manner, which serves to predict context. Efficient heading retrieval and context recognition correlate with rate changes reflecting integration of featural and geometric information in the active ensemble. These data illustrate how context recognition and heading retrieval are coded in CA1 and how these processes change with experience.

Familiarity enhances functional connectivity between visual and nonvisual regions of the brain during natural viewing.

We explored the neural correlates of familiarity with people and places using a naturalistic viewing paradigm. Neural responses were measured using functional magnetic resonance imaging, while participants viewed a movie taken from Game of Thrones. We compared inter-subject correlations and functional connectivity in participants who were either familiar or unfamiliar with the TV series. Higher inter-subject correlations were found between familiar participants in regions, beyond the visual brain, that are typically associated with the processing of semantic, episodic, and affective information. However, familiarity also increased functional connectivity between face and scene regions in the visual brain and the nonvisual regions of the familiarity network. To determine whether these regions play an important role in face recognition, we measured responses in participants with developmental prosopagnosia (DP). Consistent with a deficit in face recognition, the effect of familiarity was significantly attenuated across the familiarity network in DP. The effect of familiarity on functional connectivity between face regions and the familiarity network was also attenuated in DP. These results show that the neural response to familiarity involves an extended network of brain regions and that functional connectivity between visual and nonvisual regions of the brain plays an important role in the recognition of people and places during natural viewing.

Event-related potentials during encoding coincide with subsequent forced-choice mnemonic discrimination.

Computational models and eye-tracking research suggest that encoding variability accounts for the reduced recognition of targets (A) when paired with non-corresponding lures (B') relative to corresponding lures (A'). The current study examined whether neural activity during learning coincided with subsequent performance on the forced-choice Mnemonic Similarity Task (MST). Event-related potential responses were collected during encoding while young adults completed A-B' and A-A' trials of the forced-choice MST. Consistent with previous research, performance was lower on A-B' trials than A-A' trials. The subsequent memory effect was not significant for the A-A' test format. However, for A-B' trials, we observed a significant Accuracy × Stimulus interaction 1000-1200 ms poststimulus onset across frontal and fronto-central electrodes. As hypothesized, subsequently correct A-B' trials were associated with a larger amplitude response at encoding to the target (A) than the original version of the non-corresponding lure (B). However, subsequently incorrect trials were associated with a larger amplitude response to the non-corresponding lure (B) than the target stimulus (A). These findings provide additional support for the effect of encoding variability on mnemonic discrimination.

A familiar face and person processing area in the human temporal pole.

How does the brain process the faces of familiar people? Neuropsychological studies have argued for an area of the temporal pole (TP) linking faces with person identities, but magnetic susceptibility artifacts in this region have hampered its study with fMRI. Using data acquisition and analysis methods optimized to overcome this artifact, we identify a familiar face response in TP, reliably observed in individual brains. This area responds strongly to visual images of familiar faces over unfamiliar faces, objects, and scenes. However, TP did not just respond to images of faces, but also to a variety of high-level social cognitive tasks, including semantic, episodic, and theory of mind tasks. The response profile of TP contrasted with a nearby region of the perirhinal cortex that responded specifically to faces, but not to social cognition tasks. TP was functionally connected with a distributed network in the association cortex associated with social cognition, while PR was functionally connected with face-preferring areas of the ventral visual cortex. This work identifies a missing link in the human face processing system that specifically processes familiar faces, and is well placed to integrate visual information about faces with higher-order conceptual information about other people. The results suggest that separate streams for person and face processing reach anterior temporal areas positioned at the top of the cortical hierarchy.

Language-general versus language-specific processes in bilingual voice learning.

Language experience confers a benefit to voice learning, a concept described in the literature as the language familiarity effect (LFE). What experiences are necessary for the LFE to be conferred is less clear. We contribute empirically and theoretically to this debate by examining within and across language voice learning with Cantonese-English bilingual voices in a talker-voice association paradigm. Listeners were trained in Cantonese or English and assessed on their abilities to generalize voice learning at test on Cantonese and English utterances. By testing listeners from four language backgrounds - English Monolingual, Cantonese-English Multilingual, Tone Multilingual, and Non-tone Multilingual groups - we assess whether the LFE and group-level differences in voice learning are due to varying abilities (1) in accessing the relative acoustic-phonetic features that distinguish a voice, (2) learning at a given rate, or (3) generalizing learning of talker-voice associations to novel same-language and different-language utterances. The specific four language background groups allow us to investigate the roles of language-specific familiarity, tone language experience, and generic multilingual experience in voice learning. Differences in performance across listener groups shows evidence in support of the LFE and the role of two mechanisms for voice learning: the extraction and association of talker-specific, language-general information that is more robustly generalized across languages, and talker-specific, language-specific information that may be more readily accessible and learnable, but due to its language-specific nature, is less able to be extended to another language.

Prosodic discrimination skills mediate the association between musical aptitude and vocal emotion recognition ability.

The current study tested the hypothesis that the association between musical ability and vocal emotion recognition skills is mediated by accuracy in prosody perception. Furthermore, it was investigated whether this association is primarily related to musical expertise, operationalized by long-term engagement in musical activities, or musical aptitude, operationalized by a test of musical perceptual ability. To this end, we conducted three studies: In Study 1 (N = 85) and Study 2 (N = 93), we developed and validated a new instrument for the assessment of prosodic discrimination ability. In Study 3 (N = 136), we examined whether the association between musical ability and vocal emotion recognition was mediated by prosodic discrimination ability. We found evidence for a full mediation, though only in relation to musical aptitude and not in relation to musical expertise. Taken together, these findings suggest that individuals with high musical aptitude have superior prosody perception skills, which in turn contribute to their vocal emotion recognition skills. Importantly, our results suggest that these benefits are not unique to musicians, but extend to non-musicians with high musical aptitude.

Mice integrate conspecific and contextual information in forming social episodic-like memories under spontaneous recognition task conditions.

The ability to remember unique past events (episodic memory) may be an evolutionarily conserved function, with accumulating evidence of episodic-(like) memory processing in rodents. In humans, it likely contributes to successful complex social networking. Rodents, arguably the most used laboratory models, are also rather social animals. However, many behavioural paradigms are devoid of sociality, and commonly-used social spontaneous recognition tasks (SRTs) are open to non-episodic strategies based upon familiarity. We address this gap by developing new SRT variants. Here, in object-in-context SRTs, we asked if context could be specified by the presence/absence of either a conspecific (experiment 1) or an additional local object (experiment 2). We show that mice readily used the conspecific as contextual information to distinguish unique episodes in memory. In contrast, no coherent behavioural response emerged when an additional object was used as a potential context specifier. Further, in a new social conspecific-in-context SRT (experiment 3) where environment-based change was the context specifier, mice preferably explored a more recently-seen familiar conspecific associated with contextual mismatch, over a less recently-seen familiar conspecific presented in the same context. The results argue that, in incidental SRT conditions, mice readily incorporate conspecific cue information into episodic-like memory. Thus, the tasks offer different ways to assess and further understand the mechanisms at work in social episodic-like memory processing.

Chemogenetic activation of histamine neurons promotes retrieval of apparently lost memories.

Memory retrieval can become difficult over time, but it is important to note that memories that appear to be forgotten might still be stored in the brain, as shown by their occasional spontaneous retrieval. Histamine in the central nervous system is a promising target for facilitating the recovery of memory retrieval. Our previous study demonstrated that histamine H3 receptor (H3R) inverse agonists/antagonists, activating histamine synthesis and release, enhance activity in the perirhinal cortex and help in retrieving forgotten long-term object recognition memories. However, it is unclear whether enhancing histaminergic activity alone is enough for the recovery of memory retrieval, considering that H3Rs are also located in other neuron types and affect the release of multiple neurotransmitters. In this study, we employed a chemogenetic method to determine whether specifically activating histamine neurons in the tuberomammillary nucleus facilitates memory retrieval. In the novel object recognition test, control mice did not show a preference for objects based on memory 1 week after training, but chemogenetic activation of histamine neurons before testing improved memory retrieval. This selective activation did not affect the locomotor activity or anxiety-related behavior. Administering an H2R antagonist directly into the perirhinal cortex inhibited the recovery of memory retrieval induced by the activation of histamine neurons. Furthermore, we utilized the Barnes maze test to investigate whether chemogenetic activation of histamine neurons influences the retrieval of forgotten spatial memories. Control mice explored all the holes in the maze equally 1 week after training, whereas mice with chemogenetically activated histamine neurons spent more time around the target hole. These findings indicate that chemogenetic activation of histamine neurons in the tuberomammillary nucleus can promote retrieval of seemingly forgotten object recognition and spatial memories.

A dual mechanisms of control account of age differences in working memory.

Age-related differences in working memory (WM) can be large, but the exact sources are unclear. We hypothesized that young adults outperform older adults on WM tasks because they use controlled attention processes to prioritize the maintenance of relevant information in WM in a proactive mode, whereas older adults tend to rely on the strength of familiarity signals to make memory decisions in a reactive mode. We used a WM task that cued participants to prioritize one item over others and presented repeated lure probes that cause errors when one is engaged in a reactive mode. Results showed that, relative to young adults with full attention available to use proactive control during the delays, older adults with full attention (and young adults with divided attention) during the delays had exaggerated error rates to repeated lure probes compared to control probes. When the amount of proactive interference was increased (by repeating stimuli across trials), older adults were able to engage in proactive control, and this eliminated their exaggerated error rate (while young adults with divided attention could not). These results provide evidence for a dual mechanisms of control account of age differences in WM. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Unveiling the neural dynamics of conscious perception in rapid object recognition.

Our brain excels at recognizing objects, even when they flash by in a rapid sequence. However, the neural processes determining whether a target image in a rapid sequence can be recognized or not remains elusive. We used electroencephalography (EEG) to investigate the temporal dynamics of brain processes that shape perceptual outcomes in these challenging viewing conditions. Using naturalistic images and advanced multivariate pattern analysis (MVPA) techniques, we probed the brain dynamics governing conscious object recognition. Our results show that although initially similar, the processes for when an object can or cannot be recognized diverge around 180 ms post-appearance, coinciding with feedback neural processes. Decoding analyses indicate that gist perception (partial conscious perception) can occur at ∼120 ms through feedforward mechanisms. In contrast, object identification (full conscious perception of the image) is resolved at ∼190 ms after target onset, suggesting involvement of recurrent processing. These findings underscore the importance of recurrent neural connections in object recognition and awareness in rapid visual presentations.

A general ability for judging simple and complex ensembles.

People can report summary statistics for various features about a group of objects. One theory is that different abilities support ensemble judgments about low-level features like color versus high-level features like identity. Existing research mostly evaluates such claims based on evidence of correlations within and between feature domains. However, correlations between two identical tasks that only differ in the type of feature that is used can be inflated by method variance. Another concern is that conclusions about high-level features are mostly based on faces. We used latent variable methods on data from 237 participants to investigate the abilities supporting low-level and high-level feature ensemble judgments. Ensemble judgment was measured with six distinct tests, each requiring judgments for a distinct low-level or high-level feature, using different task requirements. We also controlled for other general visual abilities when examining how low-level and high-level ensemble abilities relate to each other. Confirmatory factor analyses showed a perfect correlation between the two factors, suggesting a single ability. There was a unique relationship between these two factors beyond the influence of object recognition and perceptual speed. Additional results from 117 of the same participants also ruled out the role of working memory. This study provides strong evidence of a general ensemble judgment ability across a wide range of features at the latent level and characterizes its relationship to other visual abilities. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Recognition of facial expressions of emotions in tactile drawings by blind children, children with low vision and sighted children.

In the context of blindness, studies on the recognition of facial expressions of emotions by touch are essential to define the compensatory touch abilities and to create adapted tools on emotions. This study is the first to examine the effect of visual experience in the recognition of tactile drawings of facial expressions of emotions by children with different visual experiences. To this end, we compared the recognition rates of tactile drawings of emotions between blind children, children with low vision and sighted children aged 6-12 years. Results revealed no effect of visual experience on recognition rates. However, an effect of emotions and an interaction effect between emotions and visual experience were found. Indeed, while all children had a low average recognition rate, the drawings of fear, anger and disgust were particularly poorly recognized. Moreover, sighted children were significantly better at recognizing the drawings of surprise and sadness than the blind children who only showed high recognition rates for joy. The results of this study support the importance of developing emotion tools that can be understood by children with different visual experiences.

Perceptual narrowing continues throughout childhood: Evidence from specialization of face processing.

Face recognition shows a long trajectory of development and is known to be closely associated with the development of social skills. However, it is still debated whether this long trajectory is perceptually based and what the role is of experience-based refinements of face representations throughout development. We examined the effects of short and long-term experienced stimulus history on face processing, using regression biases of face representations towards the experienced mean. Children and adults performed same-different judgments in a serial discrimination task where two consecutive faces were drawn from a distribution of morphed faces. The results show that face recognition continues to improve after 9 years of age, with more pronounced improvements for own-race faces. This increased narrowing with age is also indicated by similar use of stimulus statistics for own-race and other-race faces in children, contrary to the different use of the overall stimulus history for these two face types in adults. Increased face proficiency in adulthood renders the perceptual system less tuned to other-race face statistics. Altogether, the results demonstrate associations between levels of specialization and the extent to which perceptual representations become narrowly tuned with age.

Low rate hippocampal delay period activity encodes behavioral experience.

Remembering what just happened is a crucial prerequisite to form long-term memories but also for establishing and maintaining working memory. So far there is no general agreement about cortical mechanisms that support short-term memory. Using a classifier-based decoding approach, we report that hippocampal activity during few sparsely distributed brief time intervals contains information about the previous sensory motor experience of rodents. These intervals are characterized by only a small increase of firing rate of only a few neurons. These low-rate predictive patterns are present in both working memory and non-working memory tasks, in two rodent species, rats and Mongolian gerbils, are strongly reduced for rats with medial entorhinal cortex lesions, and depend on the familiarity of the sensory-motor context.

Face recognition's practical relevance: Social bonds, not social butterflies.

Research on individual differences in face recognition has provided important foundational insights: their broad range, cognitive specificity, strong heritability, and resilience to change. Elusive, however, has been the key issue of practical relevance: do these individual differences correlate with aspects of life that go beyond the recognition of faces, per se? Though often assumed, especially in social realms, such correlates remain largely theoretical, without empirical support. Here, we investigate an array of potential social correlates of face recognition. We establish social relationship quality as a reproducible correlate. This link generalises across face recognition tasks and across independent samples. In contrast, we detect no robust association with the sheer quantity of social connections, whether measured directly via number of social contacts or indirectly via extraversion-related personality indices. These findings document the existence of a key social correlate of face recognition and provide some of the first evidence to support its practical relevance. At the same time, they challenge the naive assumption that face recognition relates equally to all social outcomes. In contrast, they suggest a focused link of face recognition to the quality, not quantity, of one's social connections.

Subpopulations of neurons in the perirhinal cortex enable both modality-specific and modality-invariant recognition of objects.

The perirhinal cortex (PER) supports multimodal object recognition, but how multimodal information of objects is integrated within the PER remains unknown. Here, we recorded single units within the PER while rats performed a PER-dependent multimodal object-recognition task. In this task, audiovisual cues were presented simultaneously (multimodally) or separately (unimodally). We identified 2 types of object-selective neurons in the PER: crossmodal cells, showing constant firing patterns for an object irrespective of its modality, and unimodal cells, showing a preference for a specific modality. Unimodal cells further dissociated unimodal and multimodal versions of the object by modulating their firing rates according to the modality condition. A population-decoding analysis confirmed that the PER could perform both modality-invariant and modality-specific object decoding-the former for recognizing an object as the same in various conditions and the latter for remembering modality-specific experiences of the same object.

Witnessing-condition information differentially affects evaluations of high- and moderate-confidence eyewitness identifications.

Recent research on the eyewitness confidence-accuracy relationship reveals that confidence can be highly diagnostic of accuracy when the identification evidence is collected using pristine procedures (Wixted & Wells, 2017) and in the absence of suspect bias (Smalarz, 2021). Some researchers have further argued that eyewitnesses who make high-confidence suspect identifications are highly likely to be accurate even if they experienced suboptimal witnessing conditions (Semmler et al., 2018). The current research examined evaluations of eyewitness identification evidence in cases involving suboptimal witnessing conditions. Students (Experiments 1 & 2) and community members (Experiment 3) read eight crime vignettes involving an eyewitness's identification. We manipulated information about poor witnessing conditions (present vs. absent), the eyewitness's confidence level (high vs. moderate), and the format of the confidence statement (verbal vs. numeric) and measured evaluations of eyewitness-identification accuracy. Across all three experiments, information about suboptimal witnessing conditions disproportionately reduced evaluators' belief of highly confident compared to moderately confident eyewitnesses. This differential-discrediting pattern occurred for both numeric and verbal confidence-statement formats. Expert testimony describing the imperviousness of high-confidence suspect-identification accuracy to suboptimal witnessing conditions reduced, but did not eliminate, the differential-discrediting effect. Given that crime eyewitnesses frequently experience suboptimal witnessing conditions (e.g., Behrman & Davey, 2001; Wright & McDaid, 1996), the current findings have widespread implications for the capacity of the legal system to correctly classify suspects as guilty or innocent based on eyewitness identification testimony.

How schema knowledge influences memory in older adults: Filling in the gaps, or leading memory astray?

Age-related declines in episodic memory do not affect all types of mnemonic information equally: when to-be-remembered information is in line with one's prior knowledge, or schema-congruent, older adults often show no impairments. There are two major accounts of this effect: One proposes that schemas compensate for memory failures in aging, and the other proposes that schemas instead actively impair older adults' otherwise intact memory for incongruent information. However, the evidence thus far is inconclusive, likely due to methodological constraints in teasing apart these complex underlying dynamics. We developed a paradigm that separately examines the contributions of underlying memory and schema knowledge to a final memory decision, allowing these dynamics to be examined directly. In the present study, healthy older and younger adults first searched for target objects in congruent or incongruent locations within scenes. In a subsequent test, participants indicated where in each scene the target had been located previously, and provided confidence-based recognition memory judgments that indexed underlying memory, in terms of recollection and familiarity, for the background scenes. We found that age-related increases in schema effects on target location spatial recall were predicted and statistically mediated by age-related increases in underlying memory failures, specifically within recollection. We also found that, relative to younger adults, older adults had poorer spatial memory precision within recollected scenes but slightly better precision within familiar scenes-and age increases in schema bias were primarily exhibited within recollected scenes. Interestingly, however, there were also slight age-related increases in schema effects that could not be explained by memory deficits alone, outlining a role for active schema influences as well. Together, these findings support the account that age-related schema effects on memory are compensatory in that they are driven primarily by underlying memory failures, and further suggest that age-related deficits in memory precision may also drive schema effects.

Up-regulating GABA transporter-3 in the zona incerta prevents surgery-induced memory impairment in mice.

Clinical surgery can lead to severe neuroinflammation and cognitive dysfunctions. It has been reported that astrocytes mediate memory formation and postoperative cognitive dysfunction (POCD), however, the thalamic mechanism of astrocytes in mediating POCD remains unknown. Here, we report that reactive astrocytes in zona incerta (ZI) mediate surgery-induced recognition memory impairment in male mice. Immunostaining results showed that astrocytes are activated with GABA transporter-3 (GAT-3) being down-expressed, and neurons were suppressed in the ZI. Besides, our work revealed that reactive astrocytes caused increased tonic current in ZI neurons. Up-regulating the expression of GAT-3 in astrocytes ameliorates surgery-induced recognition memory impairment. Together, our work demonstrates that the reactive astrocytes in the ZI play a crucial role in surgery-induced memory impairment, which provides a new target for the treatment of surgery-induced neural dysfunctions.