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A transthalamic pathway crucial for perception

Author

Listed:
  • Christina Mo

    (University of Melbourne
    University of Chicago)

  • Claire McKinnon

    (University of Chicago)

  • S. Murray Sherman

    (University of Chicago)

Abstract

Perception is largely supported by cortical processing that involves communication among multiple areas, typically starting with primary sensory cortex and then involving higher order cortices. This communication is served in part by transthalamic (cortico-thalamo-cortical) pathways, which ubiquitously parallel direct corticocortical pathways, but their role in sensory processing has largely remained unexplored. Here, we suggest that transthalamic processing propagates task-relevant information required for correct sensory decisions. Using optogenetics, we specifically inhibited the pathway at its synapse in higher order somatosensory thalamus of mice performing a texture-based discrimination task. We concurrently monitored the cellular effects of inhibition in primary or secondary cortex using two-photon calcium imaging. Inhibition severely impaired performance despite intact direct corticocortical projections, thus challenging the purely corticocentric map of perception. Interestingly, the inhibition did not reduce overall cell responsiveness to texture stimulation in somatosensory cortex, but rather disrupted the texture selectivity of cells, a discriminability that develops over task learning. This discriminability was more disrupted in the secondary than primary somatosensory cortex, emphasizing the feedforward influence of the transthalamic route. Transthalamic pathways may therefore act to deliver performance-relevant information to higher order cortex and are underappreciated hierarchical pathways in perceptual decision-making.

Suggested Citation

  • Christina Mo & Claire McKinnon & S. Murray Sherman, 2024. "A transthalamic pathway crucial for perception," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50163-w
    DOI: 10.1038/s41467-024-50163-w
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    References listed on IDEAS

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    1. Lauri Nurminen & Sam Merlin & Maryam Bijanzadeh & Frederick Federer & Alessandra Angelucci, 2018. "Top-down feedback controls spatial summation and response amplitude in primate visual cortex," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    2. Jerry L. Chen & Stefano Carta & Joana Soldado-Magraner & Bernard L. Schneider & Fritjof Helmchen, 2013. "Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex," Nature, Nature, vol. 499(7458), pages 336-340, July.
    3. Zengcai V. Guo & Hidehiko K. Inagaki & Kayvon Daie & Shaul Druckmann & Charles R. Gerfen & Karel Svoboda, 2017. "Maintenance of persistent activity in a frontal thalamocortical loop," Nature, Nature, vol. 545(7653), pages 181-186, May.
    4. Y. Kate Hong & Clay O. Lacefield & Chris C. Rodgers & Randy M. Bruno, 2018. "Sensation, movement and learning in the absence of barrel cortex," Nature, Nature, vol. 561(7724), pages 542-546, September.
    5. Abhishek Banerjee & Giuseppe Parente & Jasper Teutsch & Christopher Lewis & Fabian F. Voigt & Fritjof Helmchen, 2020. "Value-guided remapping of sensory cortex by lateral orbitofrontal cortex," Nature, Nature, vol. 585(7824), pages 245-250, September.
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