High baseline activity in inferior temporal cortex improves neural and behavioral discriminability during visual categorization

Spontaneous firing is a ubiquitous property of neural activity in the brain. Recent literature suggests that this baseline activity plays a key role in perception. However, it is not known how the baseline activity contributes to neural coding and behavior. Here, by recording from the single neurons in the inferior temporal cortex of monkeys performing a visual categorization task, we thoroughly explored the relationship between baseline activity, the evoked response, and behavior. Specifically we found that a low-frequency (<8 Hz) oscillation in the spike train, prior and phase-locked to the stimulus onset, was correlated with increased gamma power and neuronal baseline activity. This enhancement of the baseline activity was then followed by an increase in the neural selectivity and the response reliability and eventually a higher behavioral performance.Iran National Science Foundation (INSF

Genetic influence is linked to cortical morphology in category-selective areas of visual cortex

Funder: RCUK | Medical Research Council (MRC); doi: https://doi.org/10.13039/501100000265Abstract: Human visual cortex contains discrete areas that respond selectively to specific object categories such as faces, bodies, and places. A long-standing question is whether these areas are shaped by genetic or environmental factors. To address this question, here we analyzed functional MRI data from an unprecedented number (n = 424) of monozygotic (MZ) and dizygotic (DZ) twins. Category-selective maps were more identical in MZ than DZ twins. Within each category-selective area, distinct subregions showed significant genetic influence. Structural MRI analysis revealed that the ‘genetic voxels’ were predominantly located in regions with higher cortical curvature (gyral crowns in face areas and sulcal fundi in place areas). Moreover, we found that cortex was thicker and more myelinated in genetic voxels of face areas, while it was thinner and less myelinated in genetic voxels of place areas. This double dissociation suggests a differential development of face and place areas in cerebral cortex

The Radial Bias: A Different Slant on Visual Orientation Sensitivity in Human and Nonhuman Primates

SummaryIt is generally assumed that sensitivity to different stimulus orientations is mapped in a globally equivalent fashion across primate visual cortex, at a spatial scale larger than that of orientation columns. However, some evidence predicts instead that radial orientations should produce higher activity than other orientations, throughout visual cortex. Here, this radial orientation bias was robustly confirmed using (1) human psychophysics, plus fMRI in (2) humans and (3) behaving monkeys. In visual cortex, fMRI activity was at least 20% higher in the retinotopic representations of polar angle which corresponded to the radial stimulus orientations (relative to tangential). In a global demonstration of this, we activated complementary retinotopic quadrants of visual cortex by simply changing stimulus orientation, without changing stimulus location in the visual field. This evidence reveals a neural link between orientation sensitivity and the cortical retinotopy, which have previously been considered independent

A High-Light Sensitivity Optical Neural Silencer: Development and Application to Optogenetic Control of Non-Human Primate Cortex

Technologies for silencing the electrical activity of genetically targeted neurons in the brain are important for assessing the contribution of specific cell types and pathways toward behaviors and pathologies. Recently we found that archaerhodopsin-3 from Halorubrum sodomense (Arch), a light-driven outward proton pump, when genetically expressed in neurons, enables them to be powerfully, transiently, and repeatedly silenced in response to pulses of light. Because of the impressive characteristics of Arch, we explored the optogenetic utility of opsins with high sequence homology to Arch, from archaea of the Halorubrum genus. We found that the archaerhodopsin from Halorubrum strain TP009, which we named ArchT, could mediate photocurrents of similar maximum amplitude to those of Arch (∼900 pA in vitro), but with a >3-fold improvement in light sensitivity over Arch, most notably in the optogenetic range of 1–10 mW/mm2, equating to >2× increase in brain tissue volume addressed by a typical single optical fiber. Upon expression in mouse or rhesus macaque cortical neurons, ArchT expressed well on neuronal membranes, including excellent trafficking for long distances down neuronal axons. The high light sensitivity prompted us to explore ArchT use in the cortex of the rhesus macaque. Optical perturbation of ArchT-expressing neurons in the brain of an awake rhesus macaque resulted in a rapid and complete (∼100%) silencing of most recorded cells, with suppressed cells achieving a median firing rate of 0 spikes/s upon illumination. A small population of neurons showed increased firing rates at long latencies following the onset of light stimulation, suggesting the existence of a mechanism of network-level neural activity balancing. The powerful net suppression of activity suggests that ArchT silencing technology might be of great use not only in the causal analysis of neural circuits, but may have therapeutic applications

The `Parahippocampal Place Area' Responds Selectively to High Spatial Frequencies

Defining the exact mechanisms by which the brain processes visual objects and scenes remains an unresolved challenge. Valuable clues to this process have emerged from the demonstration that clusters of neurons (“modules”) in inferior temporal cortex apparently respond selectively to specific categories of visual stimuli, such as places/scenes. However, the higher-order “category-selective” response could also reflect specific lower-level spatial factors. Here we tested this idea in multiple functional MRI experiments, in humans and macaque monkeys, by systematically manipulating the spatial content of geometrical shapes and natural images. These tests revealed that visual spatial discontinuities (as reflected by an increased response to high spatial frequencies) selectively activate a well-known place-selective region of visual cortex (the “parahippocampal place area”) in humans. In macaques, we demonstrate a homologous cortical area, and show that it also responds selectively to higher spatial frequencies. The parahippocampal place area may use such information for detecting object borders and scene details during spatial perception and navigation.National Institutes of Health (U.S.) (NIH Grant R01 MH6752)National Institutes of Health (U.S.) (grant R01 EY017081)Athinoula A. Martinos Center for Biomedical ImagingNational Center for Research Resources (U.S.)Mind Research Institut

An Open Resource for Non-human 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. Unfortunately, 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 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets

Genetic influence is linked to cortical morphology in category-selective areas of visual cortex.

Human visual cortex contains discrete areas that respond selectively to specific object categories such as faces, bodies, and places. A long-standing question is whether these areas are shaped by genetic or environmental factors. To address this question, here we analyzed functional MRI data from an unprecedented number (n = 424) of monozygotic (MZ) and dizygotic (DZ) twins. Category-selective maps were more identical in MZ than DZ twins. Within each category-selective area, distinct subregions showed significant genetic influence. Structural MRI analysis revealed that the 'genetic voxels' were predominantly located in regions with higher cortical curvature (gyral crowns in face areas and sulcal fundi in place areas). Moreover, we found that cortex was thicker and more myelinated in genetic voxels of face areas, while it was thinner and less myelinated in genetic voxels of place areas. This double dissociation suggests a differential development of face and place areas in cerebral cortex

Exploring the functional organization of cerebral cortex using data from the Human Connectome Project

Neuroimaging techniques such as MRI and fMRI provide a non-invasive window to look at the macroscale organization of cerebral cortex. Despite monumental efforts to map the structure and function of cerebral cortex, our understanding has been limited due to insufficient sample sizes, low-resolution imaging, and suboptimal volume-based analyses. In recent years, the Human Connectome Project (HCP) has released high-quality imaging datasets from an unprecedented number of subjects. The surface-based analysis of HCP data provides a unique opportunity to investigate detailed topography of structural features and functional activation maps in cerebral cortex. In my thesis, I will describe three studies that were conducted using the HCP database. In the first study, I tested genetic influences on the organization of category-selective areas of visual cortex. Using fMRI data from monozygotic (MZ) and dizygotic (DZ) twins, I found that category-selective maps for faces, bodies, and places were more identical in MZ than DZ twins. Within each category-selective area, distinct subregions showed significant genetic influences. Structural MRI analysis revealed that the cortical curvature, thickness, and myelination in genetic and non-genetic subregions were different. The results suggest a link between genetic influences and cortical morphology during cortical development. In the second study, I analyzed functional activation maps in language and social tasks, and found an important link between language and social processing in the human brain. While certain cortical areas in the left hemisphere were specialized in language processing, their homologues in the right hemisphere were specialized in processing of social information. This complementary hemispheric lateralization provides novel insights into the origin of language selectivity in the brain, and it could have implications in understanding neurocognitive mechanisms of social disorders such as autism. In the third study, I comprehensively investigated the large-scale functional architecture of cerebral cortex during naturalistic movie-watching. A data-driven clustering approach revealed a map of 24 functional areas/networks, each related to a specific aspect of sensory or cognitive processing. The map included three distinct executive control (domain-general) networks which showed a strong push-pull interaction with domain-specific regions in visual, auditory, and language cortex. The cortical parcellation scheme presented here provides a comprehensive and unified map of functionally defined areas, which could replace a large set of functional localizer maps. At the end of the thesis, I outline additional ongoing projects using the HCP database, addressing a number of further questions concerning the organization of human cerebral cortex

Spatially Adjacent Regions in Posterior Cingulate Cortex Represent Familiar Faces at Different Levels of Complexity.

Extensive research has shown that perceptual information of faces is processed in a network of hierarchically-organized areas within ventral temporal cortex. For familiar and famous faces, perceptual processing of faces is normally accompanied by extraction of semantic knowledge about the social status of persons. Semantic processing of familiar faces could entail progressive stages of information abstraction. However, the cortical mechanisms supporting multistage processing of familiar faces have not been characterized. Here, using an event-related fMRI experiment, familiar faces from four celebrity groups (actors, singers, politicians, and football players) and unfamiliar faces were presented to the human subjects (both males and females) while they were engaged in a face categorization task. We systematically explored the cortical representations for faces, familiar faces, subcategories of familiar faces, and familiar face identities using whole-brain univariate analysis, searchlight-based multivariate pattern analysis (MVPA), and functional connectivity analysis. Convergent evidence from all these analyses revealed a set of overlapping regions within posterior cingulate cortex (PCC) that contained decodable fMRI responses for representing different levels of semantic knowledge about familiar faces. Our results suggest a multistage pathway in PCC for processing semantic information of faces, analogous to the multistage pathway in ventral temporal cortex for processing perceptual information of faces.SIGNIFICANCE STATEMENT Recognizing familiar faces is an important component of social communications. Previous research has shown that a distributed network of brain areas is involved in processing the semantic information of familiar faces. However, it is not clear how different levels of semantic information are represented in the brain. Here, we evaluated the multivariate response patterns across the entire cortex to discover the areas that contain information for familiar faces, subcategories of familiar faces, and identities of familiar faces. The searchlight maps revealed that different levels of semantic information are represented in topographically adjacent areas within posterior cingulate cortex (PCC). The results suggest that semantic processing of faces is mediated through progressive stages of information abstraction in PCC

Does Retinotopy Influence Cortical Folding in Primate Visual Cortex?

In humans and other Old World primates, much of visual cortex comprises a set of retinotopic maps, embedded in a cortical sheet with well known, identifiable folding patterns. However, the relationship between these two prominent cortical variables has not been comprehensively studied. Here, we quantitatively tested this relationship using functional and structural magnetic resonance imaging in monkeys and humans. We found that the vertical meridian of the visual field tends to be represented on gyri (convex folds), whereas the horizontal meridian is preferentially represented in sulci (concave folds), throughout visual cortex in both primate species. This relationship suggests that the retinotopic maps may constrain the pattern of cortical folding during development.National Institutes of Health (Grants R01 MH67529 and R01 EY017081)Martinos Center for Biomedical ImagingNational Center for Research ResourcesMIND Institut