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

Author:

Toosi Ramin12ORCID,Karami Behnam345,Koushki Roxana3,Shakerian Farideh6,Noroozi Jalaledin37,Rezayat Ehsan38,Vahabie Abdol-Hossein38,Akhaee Mohammad Ali1,Dehaqani Mohammad-Reza A.123

Affiliation:

1. School of Electrical and Computer Engineering, College of Engineering, University of Tehran

2. Cognitive Systems Laboratory, Control and Intelligent Processing Center of Excellence (CIPCE), School of Electrical and Computer Engineering, College of Engineering, University of Tehran

3. School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM)

4. Perception and Plasticity Group, German Primate Center, Leibniz Institute for Primate Research

5. Neural Circuits and Cognition Lab, European Neuroscience Institute Gottingen - A Joint Initiative of the University Medical Center Gottingen and the Max Planck Society

6. Department of Brain and Cognitive Sciences, Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, ACECR

7. Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University

8. Department of Psychology, Psychology and Educational Science Faculty, University of Tehran

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.

Publisher

eLife Sciences Publications, Ltd

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