Motor cortex gates distractor stimulus encoding in sensory cortex

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.

Goal-Directed Learning is Multidimensional and Accompanied by Diverse and Widespread Changes in Neocortical Signaling

“…Target stimuli in expertly trained mice additionally evoked activations of large swaths of frontal cortex (bilateral) and rostral-lateral parietal cortex (unilateral) (Figure 7C). In contrast, distractor stimuli in expertly trained mice evoked mild suppression throughout frontal and parietal cortices, with notably reduced propagation to ipsilateral wMC, ipsilateral RSP, and contralateral wS1 (Figure 7G) (Aruljothi et al, 2020; Zhang & Zagha, 2023).…”

“…Experimental protocols have been approved by the IACUC of University of California, Riverside. The behavioral dataset used here includes studies that have been previously reported (Aruljothi et al, 2020; Marrero et al, 2022; Zareian et al, 2023; Zareian et al, 2021; Zhang & Zagha, 2023). Wild type (C57BL/6J, JAX #000664; BALB/cByJ, JAX #001026), transgenic (Snap25-2A-GCaMP6s-D, JAX #025111; Thy1-ChR2-YFP, JAX #007612; VGAT-ChR2-EYFP, JAX #014548), and virus-injected adult male and female mice were included in the behavioral learning data.…”

Interareal Synaptic Inputs Underlying Whisking-Related Activity in the Primary Somatosensory Barrel Cortex

“…Neuronal activity in wM1 can influence wS1 activity ( Xu et al, 2012 ; Lee et al, 2013 ; Pais-Vieira et al, 2013 ; Zhang and Zagha, 2023 ). This impact can either originate directly from axonal terminals of wM1 neurons that project to wS1 ( Petreanu et al, 2009 , 2012 ; Lee et al, 2013 ; Zagha et al, 2013 ; Kinnischtzke et al, 2014 ; Naskar et al, 2021 ) or indirectly through signaling from other brain areas ( Urbain and Deschênes, 2007b ; Pais-Vieira et al, 2013 ).…”

Stimulus selection drives value-modulated somatosensory processing in superior colliculus

“…Both brain areas receive bottom-up whisker information that encodes the location of stimuli in somatotopic coordinates. Both areas receive top-down input from motor and association cortices, providing a circuit basis for contextualizing stimulus information with goal-oriented actions [13][14][15][16]. S1 provides monosynaptic sensory drive to SC, and ascending SC projections to the thalamus augment whisker responses in S1, forming a reciprocal flow of tactile information [13,17,18].…”