Dorsolateral striatum, not motor cortex, is a bottleneck for responding to task-relevant stimuli in a learned whisker detection task in mice

Abstract

A learned sensory-motor behavior engages multiple brain regions, including the neocortex and the basal ganglia. How these brain regions coordinate to affect sensory selection (for target stimuli) and inhibition (for distractor stimuli) remains unknown. Here, we performed laminar electrophysiological recordings and muscimol inactivation in frontal cortex and dorsolateral striatum to determine the representations within and functions of each region during selective detection performance. From the recording experiments, in deep layers of frontal cortex and dorsolateral striatum we observed similar encoding of sensory and motor features. However, muscimol inactivation of each region resulted in drastically different outcomes. Inactivation of target-aligned striatum substantially reduced behavioral responses to all task stimuli without disrupting the ability to respond, suggesting essential roles in sensory selection. In contrast, inactivation of distractor-aligned frontal cortex increased responses to distractor stimuli, indicating essential roles in distractor inhibition. Overall, these data suggest distinct functions of frontal cortex and dorsolateral striatum in this task, despite having similar neuronal representations.

Frontal Cortex Gates Distractor Stimulus Encoding in Sensory Cortex

“…Additionally, we have considered why ‘spillover’ of distractor responses into target-aligned S1 would impair distractor response suppression. In a concurrent study (Zareian et al, 2022), we demonstrate that activation of target-aligned dorsolateral striatum (DLS) is critical for response triggering, for both target and distractor stimuli. Whisker-evoked responses propagate widely and across hemispheres in naïve rodents (Aronoff et al, 2010; Aruljothi et al, 2020; Ferezou et al, 2007; Pala & Stanley, 2022).…”

“…For combined behavioral-physiological studies, an important consideration is whether the task-related neuronal signals could be fully or partially accounted for by movement (Zagha et al, 2022). A specific concern for our study is whether the apparent asymmetric stimulus selectivity, and its modulations by wMC, is instead reflecting movement on 'Go' trials in our Go/No-Go task design (which are more prevalent on target than distractor trials in expert mice, Aruljothi et al, 2020).…”

“…Given the lateralization of the sensorimotor system in the mouse brain, this task establishes clear assignments of target-aligned and distractor-aligned hemispheres, contralateral to the site of sensory stimulation. Using this task, we previously demonstrated similar target and distractor stimulus encoding in their center receptive fields within the whisker region of primary somatosensory cortex (S1), yet highly attenuated propagation of distractor stimulus responses to frontal cortex (Aruljothi et al, 2020; Zareian et al, 2022). Here, we focus on top-down inputs onto S1 from whisker motor cortex (wMC), which is the frontal cortex region most densely connected to S1.…”

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

“…Experimental protocols have been approved by the IACUC of University of California, Riverside. The dataset used here include behavioral studies that have been previously reported (Aruljothi et al, 2020; Marrero et al, 2022; Zareian et al, 2022; Zareian et al, 2021; Zhang & Zagha, 2022). A wide variety of wild type and transgenic mice were considered for behavioral learning data.…”