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The Spatial Frequency Representation Predicts Category Coding in the Inferior Temporal Cortex

View ORCID ProfileRamin Toosi, Behnam Karami, Roxana Koushki, Farideh Shakerian, Jalaledin Noroozi, Ehsan Rezayat, Abdol-Hossein Vahabie, Mohammad Ali Akhaee, Mohammad-Reza A. Dehaqani
doi: https://doi.org/10.1101/2023.11.07.566068
Ramin Toosi
1School of Electrical and Computer Engineering, College of Engineering, University of Tehran, Tehran, Iran
2Cognitive Systems Laboratory, Control and Intelligent Processing Center of Excellence (CIPCE), School of Electrical and Computer Engineering, College of Engineering, University of Tehran, Tehran, Iran
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  • ORCID record for Ramin Toosi
Behnam Karami
3School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran
4Perception and Plasticity Group, German Primate Center, Leibniz Institute for Primate Research, 37077 Gottingen, Germany
5Neural Circuits and Cognition Lab, European Neuroscience Institute Gottingen - A Joint Initiative of the University Medical Center Gottingen and the Max Planck Society, 37077 Gottingen, Germany
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Roxana Koushki
3School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran
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Farideh Shakerian
6Department of Brain and Cognitive Sciences, Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, ACECR, Tehran, Iran
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Jalaledin Noroozi
3School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran
7Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
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Ehsan Rezayat
3School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran
8Department of Psychology, Psychology and Educational Science Faculty, University of Tehran, Tehran, Iran
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Abdol-Hossein Vahabie
3School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran
8Department of Psychology, Psychology and Educational Science Faculty, University of Tehran, Tehran, Iran
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Mohammad Ali Akhaee
1School of Electrical and Computer Engineering, College of Engineering, University of Tehran, Tehran, Iran
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  • For correspondence: [email protected] [email protected]
Mohammad-Reza A. Dehaqani
1School of Electrical and Computer Engineering, College of Engineering, University of Tehran, Tehran, Iran
2Cognitive Systems Laboratory, Control and Intelligent Processing Center of Excellence (CIPCE), School of Electrical and Computer Engineering, College of Engineering, University of Tehran, Tehran, Iran
3School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran
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  • For correspondence: [email protected] [email protected]
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Abstract

Understanding the neural representation of spatial frequency (SF) in the primate cortex is vital for unraveling visual processing mechanisms in object recognition. While numerous studies concentrate on the representation of SF in the primary visual cortex, the characteristics of SF representation and its interaction with category representation remain inadequately understood. To explore SF representation in the inferior temporal (IT) cortex of macaque monkeys, we conducted extracellular recordings with complex stimuli systematically filtered by SF. Our findings disclose an explicit SF coding at single-neuron and population levels in the IT cortex. Moreover, the coding of SF content exhibits a coarse-to-fine pattern, declining as the SF increases. Temporal dynamics analysis of SF representation reveals that low SF (LSF) is decoded faster than high SF (HSF), and the SF preference dynamically shifts from LSF to HSF over time. Additionally, the SF representation for each neuron forms a profile that predicts category selectivity at the population level. IT neurons can be clustered into four groups based on SF preference, each exhibiting different category coding behaviors. Particularly, HSF-preferred neurons demonstrate the highest category decoding performance for face stimuli. Despite the existing connection between SF and category coding, we have identified uncorrelated representations of SF and category. In contrast to the category coding, SF is more sparse and places greater reliance on the representations of individual neurons. Comparing SF representation in the IT cortex to deep neural networks, we observed no relationship between SF representation and category coding. However, SF coding, as a category-orthogonal property, is evident across various ventral stream models. These results dissociate the separate representations of SF and object category, underscoring the pivotal role of SF in object recognition.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • In the revised manuscript, several key improvements have been made: analysis with a longer exposure time (200ms) to address contrast sensitivity concerns, efforts to improve category selectivity, matching of stimulus power in terms of spatial frequency (SF) and category, and a discussion on how convolutional neural networks (CNNs) do not capture the complexities of SF processing in the IT cortex. These revisions strengthen the findings on SF bias in IT neurons and provide a more comprehensive analysis of category coding and stimulus processing.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted April 12, 2024.
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The Spatial Frequency Representation Predicts Category Coding in the Inferior Temporal Cortex
Ramin Toosi, Behnam Karami, Roxana Koushki, Farideh Shakerian, Jalaledin Noroozi, Ehsan Rezayat, Abdol-Hossein Vahabie, Mohammad Ali Akhaee, Mohammad-Reza A. Dehaqani
bioRxiv 2023.11.07.566068; doi: https://doi.org/10.1101/2023.11.07.566068
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The Spatial Frequency Representation Predicts Category Coding in the Inferior Temporal Cortex
Ramin Toosi, Behnam Karami, Roxana Koushki, Farideh Shakerian, Jalaledin Noroozi, Ehsan Rezayat, Abdol-Hossein Vahabie, Mohammad Ali Akhaee, Mohammad-Reza A. Dehaqani
bioRxiv 2023.11.07.566068; doi: https://doi.org/10.1101/2023.11.07.566068

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