Temporal Dynamics of Neural Responses in Human Visual Cortex.

Iris I A Groen, Giovanni Piantoni, Stephanie Montenegro, Adeen Flinker, Sasha Devore, Orrin Devinsky, Werner Doyle, Patricia Dugan, Daniel Friedman, Nick F Ramsey, Natalia Petridou, Jonathan Winawer

Journal: The Journal of neuroscience : the official journal of the Society for Neuroscience 2023;42(40):7562-7580

PMID: 35999054

Abstract

Neural responses to visual stimuli exhibit complex temporal dynamics, including subadditive temporal summation, response reduction with repeated or sustained stimuli (adaptation), and slower dynamics at low contrast. These phenomena are often studied independently. Here, we demonstrate these phenomena within the same experiment and model the underlying neural computations with a single computational model. We extracted time-varying responses from electrocorticographic recordings from patients presented with stimuli that varied in duration, interstimulus interval (ISI) and contrast. Aggregating data across patients from both sexes yielded 98 electrodes with robust visual responses, covering both earlier (V1-V3) and higher-order (V3a/b, LO, TO, IPS) retinotopic maps. In all regions, the temporal dynamics of neural responses exhibit several nonlinear features. Peak response amplitude saturates with high contrast and longer stimulus durations, the response to a second stimulus is suppressed for short ISIs and recovers for longer ISIs, and response latency decreases with increasing contrast. These features are accurately captured by a computational model composed of a small set of canonical neuronal operations, that is, linear filtering, rectification, exponentiation, and a delayed divisive normalization. We find that an increased normalization term captures both contrast- and adaptation-related response reductions, suggesting potentially shared underlying mechanisms. We additionally demonstrate both changes and invariance in temporal response dynamics between earlier and higher-order visual areas. Together, our results reveal the presence of a wide range of temporal and contrast-dependent neuronal dynamics in the human visual cortex and demonstrate that a simple model captures these dynamics at millisecond resolution. Sensory inputs and neural responses change continuously over time. It is especially challenging to understand a system that has both dynamic inputs and outputs. Here, we use a computational modeling approach that specifies computations to convert a time-varying input stimulus to a neural response time course, and we use this to predict neural activity measured in the human visual cortex. We show that this computational model predicts a wide variety of complex neural response shapes, which we induced experimentally by manipulating the duration, repetition, and contrast of visual stimuli. By comparing data and model predictions, we uncover systematic properties of temporal dynamics of neural signals, allowing us to better understand how the brain processes dynamic sensory information.

Copyright © 2022 the authors.

Address: Department of Psychology, New York University, New York, New York 10003 [email protected].; Video & Image Sense Lab, Institute for Informatics, University of Amsterdam, 1098 XH Amsterdam, The Netherlands.; Department of Neurology and Neurosurgery, Utrecht Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands.; Departments of Neurology.; Neurosurgery.; Psychiatry, New York University Grossman School of Medicine, New York, New York 10016.; Department of Radiology, Center for Image Sciences, University Medical Center Utrecht, Utrecht, 3584 CX, The Netherlands.; Department of Psychology, New York University, New York, New York 10003.
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