Understanding mesoscale visual processing through the lens of high-resolution functional MRI

Wednesday, June 1, 2022, 12:00 – 2:00 pm EDT, Zoom Session

Organizer: Shahin Nasr1,2,3; 1Massachusetts General Hospital, 2Athinoula A. Martinos Center for Biomedical Imaging, 3Harvard Medical School
Presenters: Shahin Nasr, Yulia Lazarova, Luca Vizioli, Roger Tootell

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In the past twenty years, with the increase in popularity of high-resolution neuroimaging techniques, we have witnessed a surge in the number of studies focused on understanding the fine-scale functional organization of visual system. Taking advantage of state-of-the-art technologies, these studies have narrowed the gap in our understanding of mesoscale neuronal processing in the visual cortex of humans vs. animals. In this symposium, four speakers will present their recent findings about the mesoscale functional organization of visual cortex in humans. Using various high-resolution fMRI techniques they have successfully enhanced their access to the evoked activity within cortical columns across different visual areas. During the first talk, Dr. Shahin Nasr will describe his approach to his studies, based on using ultra-high field scanners combined with advanced processing pipelines to avoid spatial blurring for visualizing the columnar organization of human extrastriate visual areas (Nasr et al., 2016). In his talk, the speaker will also highlight the impact of amblyopia (lazy eye) on development of cortical columns across these areas. Accessing laminar-specific brain activity is a major step toward differentiating processing streams in visual system. In the second talk, Dr. Lazarova will present a study in which high-resolution fMRI was used to differentiate “factual vs. counterfactual” feedback streams across laminar layers of the early visual areas V1 and V2. Their findings suggest a mechanism for the coexistence of information streams and integration of feedforward and feedback processing streams (Larkum et al., 2018). Shifting our attention to the neuronal mechanism of cognitive control in higher-level visual areas, in the third talk Dr. Vizioli will present his study during which high-resolution fMRI was used to study the neuronal processing involved in active face perception. Using sub-millimeter spatial resolution provided by this technique, investigators compared the laminar profile of task-related activity modulation between V1, occipital face-selective and fusiform face-selective areas. These results provide evidence for the laminar signature of complex cognitive processes in human visual system. The interaction between the external world and the innate subject-specific criteria such as personal space plays an important role in defining the level of evoked brain activity. In the fourth talk, Dr. Roger Tootell will present a study during which high-resolution fMRI was used to reveal the columnar representation of personal and visual spaces in the human parietal cortex. Results of this study suggest that the variation in response, measured within the parietal cortical columns, is related to subjective discomfort levels during intrusion into personal space.

Presentations

Visualizing cortical columns within the retinotopic visual areas of humans with normal and amblyopic vision

Shahin Nasr1, Bryan Kennedy; 1Massachusetts General Hospital, 2Athinoula A. Martinos Center for Biomedical Imaging, 3Harvard Medical School

In the past two decades, our knowledge of cortical columns in human visual cortex has expanded considerably, thanks to advances in high-resolution functional magnetic resonance imaging (fMRI) techniques and improvements in data processing methods. In the first part of this talk, I will present the recently developed fMRI data processing techniques which have improved our capabilities to visualize cortical columns by reducing the amount of unwanted spatial blurring (Wang et al., 2021). Then, in the second part, I will demonstrate the application of these techniques in revealing the selectivity, spatial distribution, and functional connectivity of cortical columns in human retinotopic visual areas (V1-V4), including those that are involved in color, motion, stereopsis, and shape encoding (Nasr et al., 2016; Tootell and Nasr, 2017; 2020). In the third part of this talk, I will demonstrate the application of these techniques in translational studies. Specifically, I will present striking evidence for the impacts of amblyopia, a disorder caused by the interruption of balanced binocular visual inputs in early stages of life, on the fine-scale organization and the response properties of cortical columns across the retinotopic visual areas. These findings will clarify the neuronal disorders that underlie multiple perceptual impairments in amblyopic individuals including stereoblindness and distorted spatial vision. All in all, the presented findings, most of them still unpublished, will highlight the importance of studying cortical columns in understanding visual perception in humans with normal and impaired vision.

Layer-specific profiles of factual and counterfactual feedback signals in human early visual cortex during navigation – 7T fMRI study

Yulia Lazarova1, Lucy Petro1,2, Angus Paton1,2, Lars Mucli1,2; 1Centre for Cognitive NeuroImaging, School of Psychology and Neuroscience, College of Medical, Veterinary and Life Sciences, University of Glasgow, 2Imaging Centre for Excellence (ICE), College of Medical, Veterinary and Life Sciences, University of Glasgow

We rely on pre-existing models of the world stored from past experiences in order to form internal representations of our present environment. In addition to facilitating perception in the present, these models enable us to engage in prospective thoughts and mental simulations unrelated to the immediate environment, known as counterfactual thoughts. Traces of both streams have been found to share some neuronal mechanisms at the earliest level of cortical processing (Monaco, 2020; Huang, 2021). It is still a challenge to understand the mechanisms that allow the parallel existence of these two streams of thought while at the same time keeping the perception of reality and imagination segregated. We used a VR headset to familiarise participants with a virtual environment prior to scanning. We recorded 7T fMRI while participants were presented with videos simulating navigation through the environment. Directional cues elicited expectations for an upcoming room that the participant was not presently viewing, but about which they could generate prospective thoughts. The lower right quadrant of the video was hidden behind an occluder, blocking feedforward input to the corresponding patch of the visual cortex. We applied MVPA analysis to probe the contents of the activation in the non-stimulated areas of V1 and V2. The results revealed that different top-down inputs target different cortical layers depending on the type of information they carry. Our data suggests the coexistence of information streams might depend on cortical layering, and layer-spanning pyramidal neurons that integrate feedforward and feedback processing (Larkum, 2018).

Characterizing top-down related functional microcircuitry of face processing in visual cortex using ultra high field fMRI

Luca Vizioli1,2, Logan Dowdle1,2, Essa Yacoub1; 1Center for Magnetic Resonance Research, University of Minnesota, 2Department of Neurosurgery, University of Minnesota

At ultra-high field it is now possible to acquire functional images with unprecedented spatial precision, spanning the submillimeter range. These measurements allow investigations of some fundamental units of neural computations, such as cortical layers and columns, that had previously only been accessible in animals using invasive electrophysiology. With submillimeter fMRI it is therefore possible, in principle, to study fine scale organization of high-level cognitive processes that are unique to humans. Here we evaluated top-down effects of high-level, socially relevant task demands, such as face perception, across cortical depths in lower and higher-level visual areas using functional images recorded with 0.7mm isotropic voxels. To this end, we instructed participants to perform either a face detection or a stimulus-irrelevant fixation task with identical phase scrambled (ranging from 0 to 40% phase coherence) faces. Using an independent functional localizer, we identified 3 regions of interest (i.e. Fusiform and Occipital face areas and V1) and segmented each region into 3 cortical depths. To evaluate task-related top-down modulations, we calculated the ratio of the activation during the face relative to the fixation task at each cortical depth. Task-related top-down modulations were more pronounced in the inner than the outer layers of V1; and in the outer compared to the inner layers in the FFA (p<0.05). These findings are consistent with feedback exchange between deeper and superficial layers, and with apical dendritic amplification being a key mechanism of conscious perception. This work represents a promising step towards characterizing laminar functional profiles for complex human-specific cognitive processes.

Columnar Encoding of Personal Space and Visual Space in Human Parietal Cortex

Roger Tootell1,2,3, Zahra Nasiravavaki1,2, Baktash Babadi1,2, Douglas Greve1,2,3, Daphne Holt2,3,4; 1Department of Radiology, Massachusetts General Hospital, 2Athinoula A. Martinos Center for Biomedical Imaging, 3Harvard Medical School, 4Department of Psychiatry, Massachusetts General Hospital

Personal space (PS) is the distance that people prefer to maintain between themselves and unfamiliar others. Intrusion into the PS evokes discomfort, and an urge to move further apart. Behavioral aspects of PS regulation have been well studied, but the brain mechanisms underlying PS have not. Here we hypothesized that PS processing involves a known body-defensive circuit including inferior parietal cortex. We examined this hypothesis at high spatial resolution, demonstrating two categories of space-sensitive cortical columns in inferior parietal cortex, using 7T fMRI (1.1 mm isotropic). First, personal space was measured in each subject, both outside and inside the scanner. During subsequent scanning, one category of columns responded when faces were presented at virtual distances that were within (but not beyond) each subject’s personal space boundary. In the majority of columns in this category, BOLD response amplitudes increased with increasing face proximity; in remaining columns, the responses decreased. These fMRI response variations appeared related to previously-described variations in subjective discomfort levels, and physiologic arousal, during intrusion into (but not beyond) personal space. The second category of columns responded strongly to either ‘near’ or ‘far’ binocular disparity in visual space, in random dot stereograms. These disparity columns in parietal cortex were functionally similar to disparity columns described previously in occipital cortex. Topographically, the disparity-selective columns were found to be systematically interdigitated with the personal space-sensitive columns. Thus, the transformation of visual to higher-order information may be computed in multiple discrete sites, rather than in a graded fashion, across parietal cortex.

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