Literature DB >> 35999054

Temporal dynamics of neural responses in human visual cortex.

Iris I A Groen1,2, Giovanni Piantoni3, Stephanie Montenegro4, Adeen Flinker4, Sasha Devore4, Orrin Devinsky4,5,6, Werner Doyle5, Patricia Dugan4, Daniel Friedman4, Nick Ramsey3, Natalia Petridou7, Jonathan Winawer8.   

Abstract

Neural responses to visual stimuli exhibit complex temporal dynamics, including sub-additive 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 (ECoG) recordings from patients presented with stimuli that varied in contrast, duration, and inter-stimulus interval (ISI). 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 non-linear 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; response latency decreases with increasing contrast. These features are accurately captured by a computational model comprised of a small set of canonical neuronal operations: 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.SIGNIFICANCE STATEMENTSensory 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 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 that 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.

Entities:  

Year:  2022        PMID: 35999054      PMCID: PMC9546476          DOI: 10.1523/JNEUROSCI.1812-21.2022

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.709


  57 in total

1.  Enhanced temporal non-linearities in human object-related occipito-temporal cortex.

Authors:  Roy Mukamel; Michal Harel; Talma Hendler; Rafael Malach
Journal:  Cereb Cortex       Date:  2004-03-28       Impact factor: 5.357

2.  fMRI-adaptation and category selectivity in human ventral temporal cortex: regional differences across time scales.

Authors:  Kevin S Weiner; Rory Sayres; Joakim Vinberg; Kalanit Grill-Spector
Journal:  J Neurophysiol       Date:  2010-04-07       Impact factor: 2.714

3.  Relating retinotopic and object-selective responses in human lateral occipital cortex.

Authors:  Rory Sayres; Kalanit Grill-Spector
Journal:  J Neurophysiol       Date:  2008-05-07       Impact factor: 2.714

4.  Compressive spatial summation in human visual cortex.

Authors:  Kendrick N Kay; Jonathan Winawer; Aviv Mezer; Brian A Wandell
Journal:  J Neurophysiol       Date:  2013-04-24       Impact factor: 2.714

Review 5.  Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations.

Authors:  Kai J Miller; Christopher J Honey; Dora Hermes; Rajesh P N Rao; Marcel denNijs; Jeffrey G Ojemann
Journal:  Neuroimage       Date:  2013-09-07       Impact factor: 6.556

6.  Striate cortex of monkey and cat: contrast response function.

Authors:  D G Albrecht; D B Hamilton
Journal:  J Neurophysiol       Date:  1982-07       Impact factor: 2.714

7.  Different origins of gamma rhythm and high-gamma activity in macaque visual cortex.

Authors:  Supratim Ray; John H R Maunsell
Journal:  PLoS Biol       Date:  2011-04-12       Impact factor: 8.029

8.  Evaluating the correspondence between face-, scene-, and object-selectivity and retinotopic organization within lateral occipitotemporal cortex.

Authors:  Edward H Silson; Iris I A Groen; Dwight J Kravitz; Chris I Baker
Journal:  J Vis       Date:  2016       Impact factor: 2.240

9.  Neuronal synchrony and the relation between the blood-oxygen-level dependent response and the local field potential.

Authors:  Dora Hermes; Mai Nguyen; Jonathan Winawer
Journal:  PLoS Biol       Date:  2017-07-24       Impact factor: 8.029

10.  A dynamic normalization model of temporal attention.

Authors:  Rachel N Denison; Marisa Carrasco; David J Heeger
Journal:  Nat Hum Behav       Date:  2021-06-17
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