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Freiwald, W.

Publications and source records attributed to Freiwald, W..

7 recordsLinked to original sources

Iterative co-creation of harmonized human and non-human primate cellular and structural ontologies and 3D common coordinate frameworks for the basal ganglia

A major goal of the BRAIN Initiative Cell Atlas Network (BICAN) is to create a suite of foundational reference cell atlases and associated standards for human and non-human primate brains. Central to this goal is the creation of cross-species harmonized cellular taxonomies and structural parcellations with formal ontologies that can be mapped into 3D reference frameworks bridging neuroimaging and cellular and histological resolutions. We describe here an iterative approach, focused initially on the basal ganglia, to co-create structural and cellular ontologies in human, macaque and marmoset brains, including a Harmonized Ontology of Mammalian Brain Anatomy (HOMBA), and to map and refine structural parcellations into neuroimaging-based common coordinate frameworks. These references provide the framework for documenting and mapping all experimental sampling in BICAN, allowing analyses of cellular and molecular variation as a function of topographic position, and enabling comparisons of cellular, molecular and neuroimaging-based functional variation within and between primate species. HighlightsO_LIA hierarchical Harmonized Ontology of Mammalian Brain Anatomy (HOMBA) covering 2348 structures C_LIO_LIHOMBA-annotated 3D common coordinate frameworks (CCFs) of the basal ganglia across species C_LIO_LIHistologically informed 3D parcellation/atlas of 280 human subcortical structures indexed by HOMBA C_LIO_LIMapping and integration of structural, cellular and functional data with HOMBA and CCFs C_LI

neuroscience↗

A cross-species spatial transcriptomic atlas of the human and non-human primate basal ganglia

The basal ganglia are interconnected subcortical nuclei with complex topographical organization that orchestrate goal-directed behaviors and are implicated in neurodegenerative movement disorders. We generated a cellular-resolution, spatial transcriptomic atlas of the basal ganglia in human, rhesus macaque, and common marmoset, sampling over one million cells in each species. By integrating spatial data with a cross-species, consensus snRNA-seq cell type taxonomy, this atlas reveals conserved principles of molecular organization within and across structures. The cellular architecture is complex but highly stereotyped, with gene expression gradients superimposed onto discrete compartments. Extensive spatial sampling illuminates 3D gradients of molecular organization in the striatum and reveals cell type-specific core and shell compartments in the primate internal globus pallidus, which is conserved with mouse. This unified, cross-species spatial transcriptomic atlas will be a foundational resource for characterizing the molecular and functional organization of the basal ganglia and their roles in health and disease.

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Neural Synchrony Links Sensorimotor Cortices in a Network for Facial Motor Control

Primate societies rely on the production and interpretation of social signals, in particular those displayed by the face. Facial movements are controlled, according to the dominant neuropsychological schema, by two separate circuits, one originating in medial frontal cortex controlling emotional expressions, and a second one originating in lateral motor and premotor areas controlling voluntary facial movements. Despite this functional dichotomy, cortical anatomy suggests that medial and lateral areas are directly connected and may thus operate as a single network. Here we test these contrasting hypotheses through structural and functional magnetic resonance imaging (fMRI) guided electrical stimulation and simultaneous multi-channel recordings from key facial motor areas in the macaque monkey brain. These areas include medial facial motor area M3 (located in the anterior cingulate cortex); two lateral face-related motor areas: M1 (primary motor) and PMv (ventrolateral premotor); and S1 (primary somatosensory cortex). Cortical responses evoked by intracortical stimulation revealed that medial and lateral areas can exert significant functional impact on each other. Simultaneous recordings of local field potentials in all facial motor areas further confirm that during facial expressions, medial and lateral facial motor areas significantly interact, primarily in the alpha and beta frequency ranges, whereas during voluntary chewing, coupling occurs at lower frequencies. These functional interactions varied across facial movement types. Thus, at the cortical level, the control of facial movements is not mediated through independent (medial/lateral) functional streams, but results from an interacting sensorimotor network. Significance StatementPrimates communicate through facial expressions. How the brain generates facial expressions remains poorly understood. To uncover how facial motor-related cortical brain regions interact to produce facial gestures, we combined fMRI-targeted electrophysiology and intracortical microstimulation while monkeys produced qualitatively different facial movements. Our two-pronged experimental approach revealed that facial motor-related cortical areas form an interconnected network characterized by synchronized neural activity demonstrating dynamic expression-selective activity states that are coordinated across the network nodes. Thus, the multiple facial motor-related cortical areas sending axons directly into the facial nucleus operate as a single network in which the overall complex, behavior-specific inter-areal interactions dictate the relevant motor output.

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Multiple objects evoke fluctuating responses in several regions of the visual pathway

How neural representations preserve information about multiple stimuli is mysterious. Because tuning of individual neurons is coarse (for example, visual receptive field diameters can exceed perceptual resolution), the populations of neurons potentially responsive to each individual stimulus can overlap, raising the question of how information about each item might be segregated and preserved in the population. We recently reported evidence for a potential solution to this problem: when two stimuli were present, some neurons in the macaque visual cortical areas V1 and V4 exhibited fluctuating firing patterns, as if they responded to only one individual stimulus at a time (Jun et al., 2022). However, whether such an information encoding strategy is ubiquitous in the visual pathway and thus could constitute a general phenomenon remains unknown. Here we provide new evidence that such fluctuating activity is also evoked by multiple stimuli in visual areas responsible for processing visual motion (middle temporal visual area, MT), and faces (middle fundus and anterolateral face patches in inferotemporal cortex - areas MF and AL), thus extending the scope of circumstances in which fluctuating activity is observed. Furthermore, consistent with our previous results in the early visual area V1, MT exhibits fluctuations between the representations of two stimuli when these form distinguishable objects but not when they fuse into one perceived object, suggesting that fluctuating activity patterns may underlie visual object formation. Taken together, these findings point toward an updated model of how the brain preserves sensory information about multiple stimuli for subsequent processing and behavioral action. Impact StatementNeural fluctuations in multiple areas along the visual cortical hierarchy could allow the brain to represent distinct co-occurring visual stimuli.

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Emergence of brain-like mirror-symmetric viewpoint tuning in convolutional neural networks

Primates can recognize objects despite 3D geometric variations such as in-depth rotations. The computational mechanisms that give rise to such invariances are yet to be fully understood. A curious case of partial invariance occurs in the macaque face-patch AL and in fully connected layers of deep convolutional networks in which neurons respond similarly to mirror-symmetric views (e.g., left and right profiles). Why does this tuning develop? Here, we propose a simple learning-driven explanation for mirror-symmetric viewpoint tuning. We show that mirror-symmetric viewpoint tuning for faces emerges in the fully connected layers of convolutional deep neural networks trained on object recognition tasks, even when the training dataset does not include faces. First, using 3D objects rendered from multiple views as test stimuli, we demonstrate that mirror-symmetric viewpoint tuning in convolutional neural network models is not unique to faces: it emerges for multiple object categories with bilateral symmetry. Second, we show why this invariance emerges in the models. Learning to discriminate among bilaterally symmetric object categories induces reflection-equivariant intermediate representations. AL-like mirror-symmetric tuning is achieved when such equivariant responses are spatially pooled by downstream units with sufficiently large receptive fields. These results explain how mirror-symmetric viewpoint tuning can emerge in neural networks, providing a theory of how they might emerge in the primate brain. Our theory predicts that mirror-symmetric viewpoint tuning can emerge as a consequence of exposure to bilaterally symmetric objects beyond the category of faces, and that it can generalize beyond previously experienced object categories.

neuroscience↗

Efficient inverse graphics in biological face processing

Vision must not only recognize and localize objects, but perform richer inferences about the underlying causes in the world that give rise to sensory data. How the brain performs these inferences remains unknown: Theoretical proposals based on inverting generative models (or "analysis-by-synthesis") have a long history but their mechanistic implementations have typically been too slow to support online perception, and their mapping to neural circuits is unclear. Here we present a neurally plausible model for efficiently inverting generative models of images and test it as an account of one high-level visual capacity, the perception of faces. The model is based on a deep neural network that learns to invert a three-dimensional (3D) face graphics program in a single fast feedforward pass. It explains both human behavioral data and multiple levels of neural processing in non-human primates, as well as a classic illusion, the "hollow face" effect. The model fits qualitatively better than state-of-the-art computer vision models, and suggests an interpretable reverse-engineering account of how images are transformed into percepts in the ventral stream.

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An open resource for nonhuman primate imaging

Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience.\n\nUnfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers that have the necessary facilities and capabilities. The PRIMate Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design and procedures for the PRIME-DE consortium, as well as the initial release, consisting of 13 independent data collections aggregated across 11 sites (total = 98 macaque monkeys). We also outline the unique pitfalls and challenges that should be considered in the analysis of the non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.

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