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PLoS Biology Jun 2024Low and high beta frequency rhythms were observed in the motor cortex, but their respective sources and behavioral correlates remain unknown. We studied local field...
Low and high beta frequency rhythms were observed in the motor cortex, but their respective sources and behavioral correlates remain unknown. We studied local field potentials (LFPs) during pre-cued reaching behavior in macaques. They contained a low beta band (<20 Hz) dominant in primary motor cortex and a high beta band (>20 Hz) dominant in dorsal premotor cortex (PMd). Low beta correlated positively with reaction time (RT) from visual cue onset and negatively with uninstructed hand postural micro-movements throughout the trial. High beta reflected temporal task prediction, with selective modulations before and during cues, which were enhanced in moments of increased focal attention when the gaze was on the work area. This double-dissociation in sources and behavioral correlates of motor cortical low and high beta, with respect to both task-instructed and spontaneous behavior, reconciles the largely disparate roles proposed for the beta rhythm, by suggesting band-specific roles in both movement control and spatiotemporal attention.
Topics: Animals; Motor Cortex; Attention; Beta Rhythm; Movement; Reaction Time; Macaca mulatta; Male; Cues; Psychomotor Performance
PubMed: 38917200
DOI: 10.1371/journal.pbio.3002670 -
BioRxiv : the Preprint Server For... Jun 2024In the mammalian neocortex, inhibition is important for dynamically balancing excitation and shaping the response properties of cells and circuits. The various...
In the mammalian neocortex, inhibition is important for dynamically balancing excitation and shaping the response properties of cells and circuits. The various computational functions of inhibition are thought to be mediated by different inhibitory neuron types of which a large diversity exists in several species. Current understanding of the function and connectivity of distinct inhibitory neuron types has mainly derived from studies in transgenic mice. However, it is unknown whether knowledge gained from mouse studies applies to the non-human primate, the model system closest to humans. The lack of viral tools to selectively access inhibitory neuron types has been a major impediment to studying their function in the primate. Here, we have thoroughly validated and characterized several recently-developed viral vectors designed to restrict transgene expression to GABAergic cells or their parvalbumin (PV) subtype, and identified two types that show high specificity and efficiency in marmoset V1. We show that in marmoset V1 AAV-h56D induces transgene expression in GABAergic cells with up to 91-94% specificity and 79% efficiency, but this depends on viral serotype and cortical layer. AAV-PHP.eB-S5E2 induces transgene expression in PV cells across all cortical layers with up to 98% specificity and 86-90% efficiency, depending on layer. Thus, these viral vectors are promising tools for studying GABA and PV cell function and connectivity in the primate cortex.
PubMed: 38915672
DOI: 10.1101/2024.03.07.583998 -
BioRxiv : the Preprint Server For... Jun 2024In dynamic environments with volatile rewards the anterior cingulate cortex (ACC) is believed to determine whether a visual object is relevant and should be chosen. The...
In dynamic environments with volatile rewards the anterior cingulate cortex (ACC) is believed to determine whether a visual object is relevant and should be chosen. The ACC may achieve this by integrating reward information over time to estimate which objects are worth to explore and which objects should be avoided. Such a higher-order meta-awareness about which objects should be explored predicts that the ACC causally contributes to choices when the reward values of objects are unknown and must be inferred from ongoing exploration. We tested this suggestion in nonhuman primates using a learning task that varied the number of object features that could be relevant, and by controlling the motivational value of choosing objects. During learning the ACC was transiently micro-stimulated when subjects foveated the to-be-chosen stimulus. We found that stimulation selectively impaired learning when feature uncertainty and motivational value of choices were high, which was linked to a deficit in using reward outcomes for feature-specific credit assignment. Application of an adaptive reinforcement learning model confirmed a primary deficit in weighting prediction errors that led to a meta-learning impairment to adaptively increase exploration during learning and to an impaired use of working memory to support learning. These findings provide causal evidence that the reward history traces in ACC are essential for meta-adjusting the exploration-exploitation balance and the strength of working memory of object values during adaptive behavior.
PubMed: 38915609
DOI: 10.1101/2024.06.12.598723 -
BioRxiv : the Preprint Server For... Jun 2024The human cerebral cortex, pivotal for advanced cognitive functions, is composed of six distinct layers and dozens of functionally specialized areas . The layers and...
The human cerebral cortex, pivotal for advanced cognitive functions, is composed of six distinct layers and dozens of functionally specialized areas . The layers and areas are distinguished both molecularly, by diverse neuronal and glial cell subtypes, and structurally, through intricate spatial organization . While single-cell transcriptomics studies have advanced molecular characterization of human cortical development, a critical gap exists due to the loss of spatial context during cell dissociation . Here, we utilized multiplexed error-robust fluorescence in situ hybridization (MERFISH) , augmented with deep-learning-based cell segmentation, to examine the molecular, cellular, and cytoarchitectural development of human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing 16 million single cells, spans eight cortical areas across four time points in the second and third trimesters. We uncovered an early establishment of the six-layer structure, identifiable in the laminar distribution of excitatory neuronal subtypes by mid-gestation, long before the emergence of cytoarchitectural layers. Notably, while anterior-posterior gradients of neuronal subtypes were generally observed in most cortical areas, a striking exception was the sharp molecular border between primary (V1) and secondary visual cortices (V2) at gestational week 20. Here we discovered an abrupt binary shift in neuronal subtype specification at the earliest stages, challenging the notion that continuous morphogen gradients dictate mid-gestation cortical arealization . Moreover, integrating single-nuclei RNA-sequencing and in situ whole transcriptomics revealed an early upregulation of synaptogenesis in V1-specific Layer 4 neurons, suggesting a role of synaptogenesis in this discrete border formation. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This work not only provides a valuable resource for the field, but also establishes a spatially resolved single-cell analysis paradigm that paves the way for a comprehensive developmental atlas of the human brain.
PubMed: 38915567
DOI: 10.1101/2024.06.05.597673 -
PloS One 2024Visual processing relies on the identification of both local and global features of visual stimuli. While well investigated at the behavioral level, the underlying brain...
Visual processing relies on the identification of both local and global features of visual stimuli. While well investigated at the behavioral level, the underlying brain mechanisms are less clear, especially in the context of aging. Using fMRI, we aimed to investigate the neural correlates underlying local and global processing in early and late adulthood. We recruited 77 healthy adults aged 19-77 who completed a visual search task based on 2-level hierarchical stimuli made of squares and/or circles. Participants were instructed to detect a target (a square) at either a local (small) or global (large) level of a hierarchical geometrical form, in the presence or absence of other hierarchical geometrical forms (distractors). At the behavioral level, we revealed high accuracy for all participants, but older participants were slower to detect local targets, specifically in presence of distractors. At the brain level, while both local and global processing were associated with occipital activation, local processing also recruited the anterior insula and dorsal anterior cingulate cortex, that are core regions of the salience network. However, while the presence of distractors in the local condition elicited specifically stronger activation within the right anterior insula for the young group, it was not observed for older participants. In addition, older participants showed less activation than younger participants in the occipital cortex, especially for the most complex conditions. Our findings suggest that the brain correlates underlying local and global processing change with aging, especially for complex visual patterns. These results are discussed in terms of top-down reduction effects from the salience network on primary visual areas, that may lead to specific difficulties to process local visual details in older adults.
Topics: Humans; Adult; Male; Female; Middle Aged; Magnetic Resonance Imaging; Aged; Young Adult; Brain Mapping; Visual Perception; Photic Stimulation; Brain; Aging; Reaction Time; Occipital Lobe
PubMed: 38905236
DOI: 10.1371/journal.pone.0303796 -
Cerebral Cortex (New York, N.Y. : 1991) Jun 2024Recent work suggests that the adult human brain is very adaptable when it comes to sensory processing. In this context, it has also been suggested that structural...
Recent work suggests that the adult human brain is very adaptable when it comes to sensory processing. In this context, it has also been suggested that structural "blueprints" may fundamentally constrain neuroplastic change, e.g. in response to sensory deprivation. Here, we trained 12 blind participants and 14 sighted participants in echolocation over a 10-week period, and used MRI in a pre-post design to measure functional and structural brain changes. We found that blind participants and sighted participants together showed a training-induced increase in activation in left and right V1 in response to echoes, a finding difficult to reconcile with the view that sensory cortex is strictly organized by modality. Further, blind participants and sighted participants showed a training induced increase in activation in right A1 in response to sounds per se (i.e. not echo-specific), and this was accompanied by an increase in gray matter density in right A1 in blind participants and in adjacent acoustic areas in sighted participants. The similarity in functional results between sighted participants and blind participants is consistent with the idea that reorganization may be governed by similar principles in the two groups, yet our structural analyses also showed differences between the groups suggesting that a more nuanced view may be required.
Topics: Humans; Blindness; Male; Adult; Female; Magnetic Resonance Imaging; Auditory Cortex; Visual Cortex; Young Adult; Neuronal Plasticity; Acoustic Stimulation; Brain Mapping; Middle Aged; Auditory Perception; Echolocation
PubMed: 38897817
DOI: 10.1093/cercor/bhae239 -
BioRxiv : the Preprint Server For... Jun 2024Neurogliaform cells are a distinct type of GABAergic cortical interneurons known for their "volume transmission" output property. However, their activity and function...
Neurogliaform cells are a distinct type of GABAergic cortical interneurons known for their "volume transmission" output property. However, their activity and function within cortical circuits remain unclear. Here, we developed two genetic tools to target these neurons and examine their function in the primary visual cortex. We found that the spontaneous activity of neurogliaform cells positively correlated with locomotion. Silencing these neurons increased spontaneous activity during locomotion and impaired visual responses in L2/3 pyramidal neurons. Furthermore, the contrast-dependent visual response of neurogliaform cells varies with their laminar location and is constrained by their morphology and input connectivity. These findings demonstrate the importance of neurogliaform cells in regulating cortical behavioral state-dependent spontaneous activity and indicate that their functional engagement during visual stimuli is influenced by their laminar positioning and connectivity.
PubMed: 38895403
DOI: 10.1101/2024.06.05.597539 -
Scientific Reports Jun 2024We show, based on the following three grounds, that the primary visual cortex (V1) is a biological direct-shortcut deep residual learning neural network (ResNet) for...
We show, based on the following three grounds, that the primary visual cortex (V1) is a biological direct-shortcut deep residual learning neural network (ResNet) for sparse visual processing: (1) We first highlight that Gabor-like sets of basis functions, which are similar to the receptive fields of simple cells in the primary visual cortex (V1), are excellent candidates for sparse representation of natural images; i.e., images from the natural world, affirming the brain to be optimized for this. (2) We then prove that the intra-layer synaptic weight matrices of this region can be reasonably first-order approximated by identity mappings, and are thus sparse themselves. (3) Finally, we point out that intra-layer weight matrices having identity mapping as their initial approximation, irrespective of this approximation being also a reasonable first-order one or not, resemble the building blocks of direct-shortcut digital ResNets, which completes the grounds. This biological ResNet interconnects the sparsity of the final representation of the image to that of its intra-layer weights. Further exploration of this ResNet, and understanding the joint effects of its architecture and learning rules, e.g. on its inductive bias, could lead to major advancements in the area of bio-inspired digital ResNets. One immediate line of research in this context, for instance, is to study the impact of forcing the direct-shortcuts to be good first-order approximations of each building block. For this, along with the -minimization posed on the basis function coefficients the ResNet finally provides at its output, another parallel one could e.g. also be posed on the weights of its residual layers.
Topics: Deep Learning; Humans; Visual Perception; Neural Networks, Computer; Primary Visual Cortex; Models, Neurological; Visual Cortex
PubMed: 38890361
DOI: 10.1038/s41598-024-62756-y -
Progress in Neurobiology Jun 2024While it is well established that sensory cortical regions traditionally thought to be unimodal can be activated by stimuli from modalities other than the dominant one,...
While it is well established that sensory cortical regions traditionally thought to be unimodal can be activated by stimuli from modalities other than the dominant one, functions of such foreign-modal activations are still not clear. Here we show that visual activations in early auditory cortex can be related to whether or not the monkeys engaged in audio-visual tasks, to the time when the monkeys reacted to the visual component of such tasks, and to the correctness of the monkeys' response to the auditory component of such tasks. These relationships between visual activations and behavior suggest that auditory cortex can be recruited for visually-guided behavior and that visual activations can prime auditory cortex such that it is prepared for processing future sounds. Our study thus provides evidence that foreign-modal activations in sensory cortex can contribute to a subject's ability to perform tasks on stimuli from foreign and dominant modalities.
PubMed: 38879074
DOI: 10.1016/j.pneurobio.2024.102637 -
Science Advances Jun 2024The human ability to perceive vivid memories as if they "float" before our eyes, even in the absence of actual visual stimuli, captivates the imagination. To determine...
The human ability to perceive vivid memories as if they "float" before our eyes, even in the absence of actual visual stimuli, captivates the imagination. To determine the neural substrates underlying visual memories, we investigated the neuronal representation of working memory content in the primary visual cortex of monkeys. Our study revealed that neurons exhibit unique responses to different memory contents, using firing patterns distinct from those observed during the perception of external visual stimuli. Moreover, this neuronal representation evolves with alterations in the recalled content and extends beyond the retinotopic areas typically reserved for processing external visual input. These discoveries shed light on the visual encoding of memories and indicate avenues for understanding the remarkable power of the mind's eye.
Topics: Animals; Neurons; Memory, Short-Term; Primary Visual Cortex; Visual Perception; Photic Stimulation; Macaca mulatta; Visual Cortex
PubMed: 38875332
DOI: 10.1126/sciadv.adk3953