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Motor cortex gates distractor stimulus encoding in sensory cortex

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  • Zhaoran Zhang

    (University of California Riverside)

  • Edward Zagha

    (University of California Riverside
    University of California Riverside)

Abstract

Suppressing responses to distractor stimuli is a fundamental cognitive function, essential for performing goal-directed tasks. A common framework for the neuronal implementation of distractor suppression is the attenuation of distractor stimuli from early sensory to higher-order processing. However, details of the localization and mechanisms of attenuation are poorly understood. We trained mice to selectively respond to target stimuli in one whisker field and ignore distractor stimuli in the opposite whisker field. During expert task performance, optogenetic inhibition of whisker motor cortex increased the overall tendency to respond and the detection of distractor whisker stimuli. Within sensory cortex, optogenetic inhibition of whisker motor cortex enhanced the propagation of distractor stimuli into target-preferring neurons. Single unit analyses revealed that whisker motor cortex (wMC) decorrelates target and distractor stimulus encoding in target-preferring primary somatosensory cortex (S1) neurons, which likely improves selective target stimulus detection by downstream readers. Moreover, we observed proactive top-down modulation from wMC to S1, through the differential activation of putative excitatory and inhibitory neurons before stimulus onset. Overall, our studies support a contribution of motor cortex to sensory selection, in suppressing behavioral responses to distractor stimuli by gating distractor stimulus propagation within sensory cortex.

Suggested Citation

  • Zhaoran Zhang & Edward Zagha, 2023. "Motor cortex gates distractor stimulus encoding in sensory cortex," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37848-4
    DOI: 10.1038/s41467-023-37848-4
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    References listed on IDEAS

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    1. Tirin Moore & Katherine M. Armstrong, 2003. "Selective gating of visual signals by microstimulation of frontal cortex," Nature, Nature, vol. 421(6921), pages 370-373, January.
    2. Marc Zirnsak & Nicholas A. Steinmetz & Behrad Noudoost & Kitty Z. Xu & Tirin Moore, 2014. "Visual space is compressed in prefrontal cortex before eye movements," Nature, Nature, vol. 507(7493), pages 504-507, March.
    3. Leopoldo Petreanu & Diego A. Gutnisky & Daniel Huber & Ning-long Xu & Dan H. O’Connor & Lin Tian & Loren Looger & Karel Svoboda, 2012. "Activity in motor–sensory projections reveals distributed coding in somatosensation," Nature, Nature, vol. 489(7415), pages 299-303, September.
    4. Ning-long Xu & Mark T. Harnett & Stephen R. Williams & Daniel Huber & Daniel H. O’Connor & Karel Svoboda & Jeffrey C. Magee, 2012. "Nonlinear dendritic integration of sensory and motor input during an active sensing task," Nature, Nature, vol. 492(7428), pages 247-251, December.
    5. Yaser Merrikhi & Kelsey Clark & Eddy Albarran & Mohammadbagher Parsa & Marc Zirnsak & Tirin Moore & Behrad Noudoost, 2017. "Spatial working memory alters the efficacy of input to visual cortex," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
    6. Andreas J. Keller & Morgane M. Roth & Massimo Scanziani, 2020. "Feedback generates a second receptive field in neurons of the visual cortex," Nature, Nature, vol. 582(7813), pages 545-549, June.
    7. David M. Schneider & Anders Nelson & Richard Mooney, 2014. "A synaptic and circuit basis for corollary discharge in the auditory cortex," Nature, Nature, vol. 513(7517), pages 189-194, September.
    8. David M. Schneider & Janani Sundararajan & Richard Mooney, 2018. "A cortical filter that learns to suppress the acoustic consequences of movement," Nature, Nature, vol. 561(7723), pages 391-395, September.
    9. 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.
    10. Ralf D. Wimmer & L. Ian Schmitt & Thomas J. Davidson & Miho Nakajima & Karl Deisseroth & Michael M. Halassa, 2015. "Thalamic control of sensory selection in divided attention," Nature, Nature, vol. 526(7575), pages 705-709, October.
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