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Mechanism underpinning the sharpening of orientation and spatial frequency selectivities in the tree shrew (Tupaia belangeri) primary visual cortex

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Abstract

Most neurons in the primary visual cortex (V1) of mammals show sharp orientation selectivity and band-pass spatial frequency tuning. Here, we examine whether sharpening of the broad tuning that exists subcortically, namely in the retina and the lateral geniculate nucleus (LGN), underlie the sharper tuning seen for both the above features in tree shrew V1. Since the transition from poor feature selectivity to sharp tuning occurs entirely within V1 in tree shrews, we examined the orientation selectivity and spatial frequency tuning of neurons within individual electrode penetrations. We found that most layer 4 and layer 2/3 neurons in the same cortical column preferred the same stimulus orientation. However, a subset of layer 3c neurons close to the layer 4 border preferred near orthogonal orientations, suggesting that layer 2/3 neurons may inherit the orientation preferences of their layer 4 input neurons and also receive cross-orientation inhibition from layer 3c neurons. We also found that layer 4 neurons showed sharper orientation selectivity at higher spatial frequencies, suggesting that attenuation of low spatial frequency responses by spatially broad inhibition acting on layer 4 inputs to layer 2/3 neurons can enhance both orientation and spatial frequency selectivities. However, in a proportion of layer 2/3 neurons, the sharper tuning of layer 2/3 neurons appeared to arise also or even mainly from inhibition specific to high spatial frequencies acting on the layer 4 inputs to layer 2/3. Overall, our results are consistent with the suggestion that in tree shrews, sharp feature selectivity in layer 2/3 can be established by intracortical mechanisms that sharpen biases observed in layer 4, which are in turn inherited presumably from thalamic afferents.

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Funding

The project was undertaken with financial support from the ARC Centre of Excellence in Integrative Brain Function, Australian Research Council (Grant no. CE140100007) and the Department of Optometry and Vision Sciences, University of Melbourne.

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Authors and Affiliations

  1. Department of Optometry and Vision Sciences, The University of Melbourne, Melbourne, Australia

    Yamni S. Mohan, Sivaram Viswanathan, Jaikishan Jayakumar, Errol K. J. Lloyd & Trichur R. Vidyasagar

  2. Centre for Computational Brain Research, IIT Madras, Chennai, India

    Jaikishan Jayakumar

  3. ARC Centre of Excellence in Integrative Brain Function, Clayton, Australia

    Trichur R. Vidyasagar

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  1. Yamni S. Mohan
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  2. Sivaram Viswanathan
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  3. Jaikishan Jayakumar
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  4. Errol K. J. Lloyd
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  5. Trichur R. Vidyasagar
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Contributions

Experiments were conceived and planned by YM, JJ and TRV. All authors participated in data collection. YM completed data analysis with assistance from SV and JJ. YM prepared the manuscript with support from TRV and EKJL. All authors provided critical feedback and helped shape the research and manuscript.

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Correspondence to Trichur R. Vidyasagar.

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There is no conflict of interest to report for this project.

Ethics approval

All experimental procedures were approved by the Florey Institute Animal Ethics committee and were conducted in accordance with the guidelines from the Animal Welfare Act 1992, The Animal Welfare Regulations (Vic) 1993 and the National Health & Medical Research Council’s Australian Code of Practice for the Care and use of Animals for Scientific Purposes (8th Edition, listed as EA28 in the NHMRC Publications Online Catalogue under ‘Animal Ethics’).

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The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Mohan, Y.S., Viswanathan, S., Jayakumar, J. et al. Mechanism underpinning the sharpening of orientation and spatial frequency selectivities in the tree shrew (Tupaia belangeri) primary visual cortex. Brain Struct Funct 227, 1265–1278 (2022). https://doi.org/10.1007/s00429-021-02445-y

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