Neural substrate for the engagement of the ventral visual stream in motor control in the macaque monkey.

The present study aimed to describe the cortical connectivity of a sector located in the ventral bank of the superior temporal sulcus in the macaque (intermediate area TEa and TEm [TEa/m]), which appears to represent the major source of output of the ventral visual stream outside the temporal lobe. The retrograde tracer wheat germ agglutinin was injected in the intermediate TEa/m in four macaque monkeys. The results showed that 58-78% of labeled cells were located within ventral visual stream areas other than the TE complex. Outside the ventral visual stream, there were connections with the memory-related medial temporal area 36 and the parahippocampal cortex, orbitofrontal areas involved in encoding subjective values of stimuli for action selection, and eye- or hand-movement related parietal (LIP, AIP, and SII), prefrontal (12r, 45A, and 45B) areas, and a hand-related dysgranular insula field. Altogether these data provide a solid substrate for the engagement of the ventral visual stream in large scale cortical networks for skeletomotor or oculomotor control. Accordingly, the role of the ventral visual stream could go beyond pure perceptual processes and could be also finalized to the neural mechanisms underlying the control of voluntary motor behavior.

Evidence for a Causal Dissociation of the McGurk Effect and Congruent Audiovisual Speech Perception via TMS to the Left pSTS.

Congruent visual speech improves speech perception accuracy, particularly in noisy environments. Conversely, mismatched visual speech can alter what is heard, leading to an illusory percept that differs from the auditory and visual components, known as the McGurk effect. While prior transcranial magnetic stimulation (TMS) and neuroimaging studies have identified the left posterior superior temporal sulcus (pSTS) as a causal region involved in the generation of the McGurk effect, it remains unclear whether this region is critical only for this illusion or also for the more general benefits of congruent visual speech (e.g., increased accuracy and faster reaction times). Indeed, recent correlative research suggests that the benefits of congruent visual speech and the McGurk effect rely on largely independent mechanisms. To better understand how these different features of audiovisual integration are causally generated by the left pSTS, we used single-pulse TMS to temporarily disrupt processing within this region while subjects were presented with either congruent or incongruent (McGurk) audiovisual combinations. Consistent with past research, we observed that TMS to the left pSTS reduced the strength of the McGurk effect. Importantly, however, left pSTS stimulation had no effect on the positive benefits of congruent audiovisual speech (increased accuracy and faster reaction times), demonstrating a causal dissociation between the two processes. Our results are consistent with models proposing that the pSTS is but one of multiple critical areas supporting audiovisual speech interactions. Moreover, these data add to a growing body of evidence suggesting that the McGurk effect is an imperfect surrogate measure for more general and ecologically valid audiovisual speech behaviors.

Both mOTS-words and pOTS-words prefer emoji stimuli over text stimuli during a lexical judgment task.

The visual word form area in the occipitotemporal sulcus (here OTS-words) is crucial for reading and shows a preference for text stimuli. We hypothesized that this text preference may be driven by lexical processing. Hence, we performed three fMRI experiments (n = 15), systematically varying participants' task and stimulus, and separately evaluated middle mOTS-words and posterior pOTS-words. Experiment 1 contrasted text with other visual stimuli to identify both OTS-words subregions. Experiment 2 utilized an fMRI adaptation paradigm, presenting compound words as texts or emojis. In experiment 3, participants performed a lexical or color judgment task on compound words in text or emoji format. In experiment 2, pOTS-words, but not mOTS-words, showed fMRI adaptation for compound words in both formats. In experiment 3, both subregions showed higher responses to compound words in emoji format. Moreover, mOTS-words showed higher responses during the lexical judgment task and a task-stimulus interaction. Multivariate analyses revealed that distributed responses in pOTS-words encode stimulus and distributed responses in mOTS-words encode stimulus and task. Together, our findings suggest that the function of the OTS-words subregions goes beyond the specific visual processing of text and that these regions are flexibly recruited whenever semantic meaning needs to be assigned to visual input.

Individual gaze shapes diverging neural representations.

Complex visual stimuli evoke diverse patterns of gaze, but previous research suggests that their neural representations are shared across brains. Here, we used hyperalignment to compare visual responses between observers viewing identical stimuli. We find that individual eye movements enhance cortical visual responses but also lead to representational divergence. Pairwise differences in the spatial distribution of gaze and in semantic salience predict pairwise representational divergence in V1 and inferior temporal cortex, respectively. This suggests that individual gaze sculpts individual visual worlds.

Dendritic spine head diameter predicts episodic memory performance in older adults.

Episodic memory in older adults is varied and perceived to rely on numbers of synapses or dendritic spines. We analyzed 2157 neurons among 128 older individuals from the Religious Orders Study and Rush Memory and Aging Project. Analysis of 55,521 individual dendritic spines by least absolute shrinkage and selection operator regression and nested model cross-validation revealed that the dendritic spine head diameter in the temporal cortex, but not the premotor cortex, improved the prediction of episodic memory performance in models containing ß amyloid plaque scores, neurofibrillary tangle pathology, and sex. These findings support the emerging hypothesis that, in the temporal cortex, synapse strength is more critical than quantity for memory in old age.

Abstract representations emerge in human hippocampal neurons during inference.

Humans have the remarkable cognitive capacity to rapidly adapt to changing environments. Central to this capacity is the ability to form high-level, abstract representations that take advantage of regularities in the world to support generalization1. However, little is known about how these representations are encoded in populations of neurons, how they emerge through learning and how they relate to behaviour2,3. Here we characterized the representational geometry of populations of neurons (single units) recorded in the hippocampus, amygdala, medial frontal cortex and ventral temporal cortex of neurosurgical patients performing an inferential reasoning task. We found that only the neural representations formed in the hippocampus simultaneously encode several task variables in an abstract, or disentangled, format. This representational geometry is uniquely observed after patients learn to perform inference, and consists of disentangled directly observable and discovered latent task variables. Learning to perform inference by trial and error or through verbal instructions led to the formation of hippocampal representations with similar geometric properties. The observed relation between representational format and inference behaviour suggests that abstract and disentangled representational geometries are important for complex cognition.

Occipital-temporal cortical tuning to semantic and affective features of natural images predicts associated behavioral responses.

In everyday life, people need to respond appropriately to many types of emotional stimuli. Here, we investigate whether human occipital-temporal cortex (OTC) shows co-representation of the semantic category and affective content of visual stimuli. We also explore whether OTC transformation of semantic and affective features extracts information of value for guiding behavior. Participants viewed 1620 emotional natural images while functional magnetic resonance imaging data were acquired. Using voxel-wise modeling we show widespread tuning to semantic and affective image features across OTC. The top three principal components underlying OTC voxel-wise responses to image features encoded stimulus animacy, stimulus arousal and interactions of animacy with stimulus valence and arousal. At low to moderate dimensionality, OTC tuning patterns predicted behavioral responses linked to each image better than regressors directly based on image features. This is consistent with OTC representing stimulus semantic category and affective content in a manner suited to guiding behavior.

Multiscale chemogenetic dissection of fronto-temporal top-down regulation for object memory in primates.

Visual object memory is a fundamental element of various cognitive abilities, and the underlying neural mechanisms have been extensively examined especially in the anterior temporal cortex of primates. However, both macroscopic large-scale functional network in which this region is embedded and microscopic neuron-level dynamics of top-down regulation it receives for object memory remains elusive. Here, we identified the orbitofrontal node as a critical partner of the anterior temporal node for object memory by combining whole-brain functional imaging during rest and a short-term object memory task in male macaques. Focal chemogenetic silencing of the identified orbitofrontal node downregulated both the local orbitofrontal and remote anterior temporal nodes during the task, in association with deteriorated mnemonic, but not perceptual, performance. Furthermore, imaging-guided neuronal recordings in the same monkeys during the same task causally revealed that orbitofrontal top-down modulation enhanced stimulus-selective mnemonic signal in individual anterior temporal neurons while leaving bottom-up perceptual signal unchanged. Furthermore, similar activity difference was also observed between correct and mnemonic error trials before silencing, suggesting its behavioral relevance. These multifaceted but convergent results provide a multiscale causal understanding of dynamic top-down regulation of the anterior temporal cortex along the ventral fronto-temporal network underpinning short-term object memory in primates.

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.

Innovative strategies for managing hallucinations by exploring effects of tDCS on source monitoring abilities.

This randomised, crossover, sham-controlled study explored the neural basis of source-monitoring, a crucial cognitive process implicated in schizophrenia. Left superior temporal gyrus (STG) and dorsolateral prefrontal cortex (DLPFC) were the key focus areas. Thirty participants without neurological or psychological disorders underwent offline sham and active tDCS sessions with specific electrode montage targeting the left STG and DLPFC. Source-monitoring tasks, reality monitoring (Hear-Imagine), internal source-monitoring (Say-Imagine), and external source monitoring (Virtual-Real) were administered. Paired t-test and estimation statistics was performed with Graphpad version 10.1.0. The Benjamini-Hochberg procedure was employed to control the false discovery rate in multiple hypothesis testing. A significant improvement in internal source monitoring tasks (p = 0.001, Cohen's d = 0.97) was observed, but reality monitoring tasks demonstrated moderate improvement (p = 0.02, Cohen's d = 0.44). The study provides insights into the neural mechanisms of source monitoring in healthy individuals and proposes tDCS as a therapeutic intervention, laying the foundation for future studies to refine tDCS protocols and develop individualized approaches to address source monitoring deficits in schizophrenia.

Intracranial EEGs evidenced visual object processing in the human medial temporal lobe subregions.

The perirhinal cortex (PRC) and parahippocampal cortex (PHC) are core regions along the visual dual-stream. The specific functional roles of the PRC and PHC and their interactions with the downstream hippocampus cortex (HPC) are crucial for understanding visual memory. Our research used human intracranial EEGs to study the neural mechanism of the PRC, PHC, and HPC in visual object encoding. Single-regional function analyses found evidence that the PRC, PHC, and HPC are activated ∼100 ms within the broad-gamma band and that the PRC was more strongly activated than either the PHC or the HPC after an object stimulus. Inter-regional analyses showed strong bidirectional interactions of the PRC with both the PHC and HPC in the low-frequency band, whereas the interactions between the PHC and HPC were not significant. These findings demonstrated the core role of the PRC in encoding visual object information and supported the hypothesis of PRC-HPC-ventral object pathway. The recruitment of the PHC and its interaction with the PRC in visual object encoding also provide new insights beyond the traditional dorsal-stream hypothesis.

A quantitative comparison of atlas parcellations on the human superior temporal sulcus.

The superior temporal sulcus (STS) has a functional topography that has been difficult to characterize through traditional approaches. Automated atlas parcellations may be one solution while also being beneficial for both dimensional reduction and standardizing regions of interest, but they yield very different boundary definitions along the STS. Here we evaluate how well machine learning classifiers can correctly identify six social cognitive tasks from STS activation patterns dimensionally reduced using four popular atlases (Glasser et al., 2016; Gordon et al., 2016; Power et al., 2011 as projected onto the surface by Arslan et al., 2018; Schaefer et al., 2018). Functional data was summarized within each STS parcel in one of four ways, then subjected to leave-one-subject-out cross-validation SVM classification. We found that the classifiers could readily label conditions when data was parcellated using any of the four atlases, evidence that dimensional reduction to parcels did not compromise functional fingerprints. Mean activation for the social conditions was the most effective metric for classification in the right STS, whereas all the metrics classified equally well in the left STS. Interestingly, even atlases constructed from random parcellation schemes (null atlases) classified the conditions with high accuracy. We therefore conclude that the complex activation maps on the STS are readily differentiated at a coarse granular level, despite a strict topography having not yet been identified. Further work is required to identify what features have greatest potential to improve the utility of atlases in replacing functional localizers.

Functional integration and segregation during semantic cognition: Evidence across age groups.

Semantic cognition is underpinned by ventral anterior temporal lobe (vATL) which encodes knowledge representations and inferior frontal gyrus (IFG), which controls activation of knowledge based on the needs of the current context. This core semantic network has been validated in substantial empirical findings in the past. However, it remains unclear how these core semantic areas dynamically communicate with each other, and with other neural networks, to achieve successful semantic processing. Here, we investigated this question by testing functional connectivity in the core semantic network during semantic tasks and whether these connections were affected by cognitive ageing. Compared to a non-semantic task, semantic tasks increased the connectivity between left and right IFGs, indicating a bilateral semantic control system. Strengthened connectivity was also found between left IFG and left vATL, and this effect was stronger in the young group. At a whole-brain scale, IFG and vATL increased their coupling with multiple-demand regions during semantic tasks, even though these areas were deactivated relative to non-semantic tasks. This suggests that the domain-general executive network contributes to semantic processing. In contrast, IFG and vATL decreased their interaction with default mode network (DMN) areas during semantic tasks, even though these areas were positively activated by the task. This suggests that DMN areas do not contribute to all semantic tasks: their activation may sometimes reflect automatic retrieval of task-irrelevant memories and associations. Taken together, our study characterizes a dynamic connectivity mechanism supporting semantic cognition within and beyond core semantic regions.

Semantic structures facilitate threat memory integration throughout the medial temporal lobe and medial prefrontal cortex.

Emotional experiences can profoundly impact our conceptual model of the world, modifying how we represent and remember a host of information even indirectly associated with that experienced in the past. Yet, how a new emotional experience infiltrates and spreads across pre-existing semantic knowledge structures (e.g., categories) is unknown. We used a modified aversive sensory preconditioning paradigm in fMRI (n = 35) to investigate whether threat memories integrate with a pre-established category to alter the representation of the entire category. We observed selective but transient changes in the representation of conceptually related items in the amygdala, medial prefrontal cortex, and occipitotemporal cortex following threat conditioning to a simple cue (geometric shape) pre-associated with a different, but related, set of category exemplars. These representational changes persisted beyond 24 h in the hippocampus and perirhinal cortex. Reactivation of the semantic category during threat conditioning, combined with activation of the hippocampus or medial prefrontal cortex, was predictive of subsequent amygdala reactivity toward novel category members at test. This provides evidence for online integration of emotional experiences into semantic categories, which then promotes threat generalization. Behaviorally, threat conditioning by proxy selectively and retroactively enhanced recognition memory and increased the perceived typicality of the semantic category indirectly associated with threat. These findings detail a complex route through which new emotional learning generalizes by modifying semantic structures built up over time and stored in memory as conceptual knowledge.

Gaze and Arrows: Does the Gaze-Following Patch in the Posterior Temporal Cortex Differentiate Social and Symbolic Spatial Cues?

The gaze-following patch (GFP) is located in the posterior temporal cortex and has been described as a cortical module dedicated to processing other people's gaze-direction in a domain-specific manner. Thus, it appears to be the neural correlate of Baron-Cohen's eye direction detector (EDD) which is one of the core modules in his mindreading system-a neurocognitive model for the theory of mind concept. Inspired by Jerry Fodor's ideas on the modularity of the mind, Baron-Cohen proposed that, among other things, the individual modules are domain specific. In the case of the EDD, this means that it exclusively processes eye-like stimuli to extract gaze-direction and that other stimuli, which may carry directional information as well, are processed elsewhere. If the GFP is indeed EDD's neural correlate, it must meet this expectation. To test this, we compared the GFP's BOLD activity during gaze-direction following with the activity during arrow-direction following in the present human fMRI study. Contrary to the expectation based on the assumption of domain specificity, we did not find a differentiation between gaze- and arrow-direction following. In fact, we were not able to reproduce the GFP as presented in the previous studies. A possible explanation is that in the present study-unlike the previous work-the gaze stimuli did not contain an obvious change of direction that represented a visual motion. Hence, the critical stimulus component responsible for the identification of the GFP in the previous experiments might have been visual motion.

Context-invariant beliefs are supported by dynamic reconfiguration of single unit functional connectivity in prefrontal cortex of male macaques.

Natural behaviors occur in closed action-perception loops and are supported by dynamic and flexible beliefs abstracted away from our immediate sensory milieu. How this real-world flexibility is instantiated in neural circuits remains unknown. Here, we have male macaques navigate in a virtual environment by primarily leveraging sensory (optic flow) signals, or by more heavily relying on acquired internal models. We record single-unit spiking activity simultaneously from the dorsomedial superior temporal area (MSTd), parietal area 7a, and the dorso-lateral prefrontal cortex (dlPFC). Results show that while animals were able to maintain adaptive task-relevant beliefs regardless of sensory context, the fine-grain statistical dependencies between neurons, particularly in 7a and dlPFC, dynamically remapped with the changing computational demands. In dlPFC, but not 7a, destroying these statistical dependencies abolished the area's ability for cross-context decoding. Lastly, correlational analyses suggested that the more unit-to-unit couplings remapped in dlPFC, and the less they did so in MSTd, the less were population codes and behavior impacted by the loss of sensory evidence. We conclude that dynamic functional connectivity between neurons in prefrontal cortex maintain a stable population code and context-invariant beliefs during naturalistic behavior.

The representation of noun-verb distinction in left posterior middle temporal gyrus: evidence from representation similarity analyses.

Nouns and verbs are fundamental grammatical building blocks of languages. A key question is whether and where the noun-verb division was represented in the brain. Previous studies mainly used univariate analyses to examine this issue. However, the interpretation of activated brain regions in univariate analyses may be confounded with general cognitive processing and/or confounding variables. We addressed these limitations by using partial representation similarity analysis (RSA) of Chinese nouns and verbs with different levels of imageability. Participants were asked to complete the 1-back grammatical class probe (GCP; an explicit measure) and the 1-back word probe (WP; an implicit measure) tasks while undergoing functional magnetic resonance imaging. RSA results showed that the activation pattern in the left posterior middle temporal gyrus (LpMTG) was significantly correlated with the grammatical class representational dissimilarity matrix in the GCP task after eliminating the potential confounding variables. Moreover, the LpMTG did not overlap with the frontal-parietal regions that were activated by verbs vs. nouns or the task effect (CRP vs. WP) in univariate analyses. These results highlight the role of LpMTG in distinguishing nouns from verbs rather than general cognitive processing.

Time to bury the chisel: a continuous dorsal association tract system.

The arcuate fasciculus may be subdivided into a tract directly connecting frontal and temporal lobes and a pair of indirect subtracts in which the fronto-temporal connection is mediated by connections to the inferior parietal lobe. This tripartition has been advanced as an improvement over the centuries-old consensus that the lateral dorsal association fibers form a continuous system with no discernible discrete parts. Moreover, it has been used as the anatomical basis for functional hypotheses regarding linguistic abilities. Ex hypothesi, damage to the indirect subtracts leads to deficits in the repetition of multi-word sequences, whereas damage to the direct subtract leads to deficits in the immediate reproduction of single multisyllabic words. We argue that this partitioning of the dorsal association tract system enjoys no special anatomical status, and the search for the anatomical substrates of linguistic abilities should not be constrained by it. Instead, the merit of any postulated partitioning should primarily be judged on the basis of whether it enlightens or obfuscates our understanding of the behavior of patients in which individual subtracts are damaged.

Speech perception following transcranial direct current stimulation (tDCS) over left superior temporal gyrus (STG) (including Wernicke's area) versus inferior frontal gyrus (IFG) (including Broca's area).

Imaging and neurocognitive studies have searched for the brain areas involved in speech perception, specifically when speech is accompanied by noise, attempting to identify the underlying neural mechanism(s). Transcranial direct current stimulation (tDCS), a noninvasive, painless cortical neuromodulation technique, has been used to either excite or inhibit brain activity in order to better understand the neural mechanism underlying speech perception in noise. In the present study, anodal (excitatory) and cathodal (inhibitory) stimulations were performed on 48 participants, either over the left Inferior Frontal Gyrus (IFG), which includes Broca's area (n = 10 anodal, and n = 10 cathodal) or over the left Superior Temporal Gyrus (STG), which includes Wernicke's area (n = 13 anodal, n = 15 cathodal). Speech perception was measured using a sentence recognition task accompanied by white noise with a signal-to-noise ratio of -10 dB. Speech perception performance was measured four times: at baseline, after each of the two sessions of stimulation (one active and one sham session, the order of which was randomized between participants), and at a two-week follow-up session. Groups receiving anodal and cathodal stimulation over the left IFG did not show an effect of stimulation type. For groups receiving left STG stimulation, anodal stimulation resulted in higher scores, regardless of whether it was given before or after sham stimulation. However, cathodal stimulation showed an effect only when active stimulation was applied following sham stimulation. These results showed that tDCS had a direct effect on improving speech perception only over left STG. Furthermore, while anodal stimulation was effective in whatever order it was given, cathodal stimulation was effective only following sham stimulation, thereby allowing some amount of training. These findings carry both theoretical and clinical implications for the relationship between the DMN's left IFG and left STG areas during speech perception accompanied by background noise.