Abstract
SummaryExecuting learned motor behaviors often requires the transformation of sensory cues into patterns of motor commands that generate appropriately timed actions. The cerebellum and thalamus are two key areas involved in shaping cortical output and movement, but the contribution of a cerebellar-thalamocortical pathway to voluntary movement initiation remains poorly understood. Here, we investigated how an auditory “go cue” transforms thalamocortical activity patterns and how these changes relate to movement initiation. Population responses in dentate/interpositus-recipient regions of motor thalamus reflect a time-locked increase in activity immediately prior to movement initiation that is temporally uncoupled from the go cue, indicative of a fixed-latency feedforward motor timing signal. Blocking cerebellar or motor thalamic output suppresses movement initiation, while stimulation triggers movements in a behavioral context-dependent manner. Our findings show how cerebellar output, via the thalamus, shapes cortical activity patterns necessary for learned context-dependent movement initiation.
Highlights
The ability to generate appropriately timed motor actions in response to sensory cues is a hallmark of mammalian motor control
The latter is supported by neuronal activity in dentate/interpositus nuclei (DN/IPN) and recipient motor thalamic regions preceding cortical activity (Nashef et al, 2018; Strick, 1976; Thach, 1975, 2014) and movement initiation (Anderson and Turner, 1991; Butler et al, 1992, 1996; Fortier et al, 1989; Harvey et al, 1979; Horne and Porter, 1980; Kurata, 2005; Macpherson et al, 1980; Mushiake and Strick, 1993; Schmied et al, 1979; Strick, 1976; van Donkelaar et al, 1999), while disrupting activity in either region alters the timing of sensory-triggered actions (Meyer-Lohmann et al, 1977; Nashef et al, 2019; Spidalieri et al, 1983; Thach, 1975; van Donkelaar et al, 2000)
We observed miss trials, likely reflecting changing levels of attention or satiation within sessions (Figure 1E; Video S1). Since both DN and IPN are implicated in motor timing and send glutamatergic projections to ventral motor thalamus (Aumann and Horne, 1996b; Bosch-Bouju et al, 2013; Gornati et al, 2018; Kuramoto et al, 2009), we sought to define the region of thalamus that receives input from DN/IPN and projects to the caudal forelimb area (CFA) of motor cortex using a dual labeling strategy (Figure 1F)
Summary
The ability to generate appropriately timed motor actions in response to sensory cues is a hallmark of mammalian motor control. Two distinct pathways could contribute to movement initiation, the cerebellar-rubrospinal tract (Asanuma et al, 1983; Gibson et al, 1985; Teune et al, 2000) or the cerebellar-thalamocortical pathway (Bostan et al, 2013; Gornati et al, 2018; Horne and Butler, 1995; Kuramoto et al, 2009; Nashef et al, 2019) The latter is supported by neuronal activity in dentate/interpositus nuclei (DN/IPN) and recipient motor thalamic regions preceding cortical activity (Nashef et al, 2018; Strick, 1976; Thach, 1975, 2014) and movement initiation (Anderson and Turner, 1991; Butler et al, 1992, 1996; Fortier et al, 1989; Harvey et al, 1979; Horne and Porter, 1980; Kurata, 2005; Macpherson et al, 1980; Mushiake and Strick, 1993; Schmied et al, 1979; Strick, 1976; van Donkelaar et al, 1999), while disrupting activity in either region alters the timing of sensory-triggered actions (Meyer-Lohmann et al, 1977; Nashef et al, 2019; Spidalieri et al, 1983; Thach, 1975; van Donkelaar et al, 2000).
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