Different contributions of preparatory activity in the basal ganglia and cerebellum for self-timing

Abstract

The ability to flexibly adjust movement timing is important for everyday life. Although the basal ganglia and cerebellum have been implicated in monitoring of supra- and sub-second intervals, respectively, the underlying neuronal mechanism remains unclear. Here, we show that in monkeys trained to generate a self-initiated saccade at instructed timing following a visual cue, neurons in the caudate nucleus kept track of passage of time throughout the delay period, while those in the cerebellar dentate nucleus were recruited only during the last part of the delay period. Conversely, neuronal correlates of trial-by-trial variation of self-timing emerged earlier in the cerebellum than the striatum. Local inactivation of respective recording sites confirmed the difference in their relative contributions to supra- and sub-second intervals. These results suggest that the basal ganglia may measure elapsed time relative to the intended interval, while the cerebellum might be responsible for the fine adjustment of self-timing.

Cerebellar neurodynamics during motor planning predict decision timing and outcome on single-trial level

“…Second, our task has a learning component, the direct relevance of which for the involved longer timescales is shown by comparison to non-learners and fish undergoing spontaneous movements in which the predictions of turn initiation and direction are not possible to the same degree ( Figure S6). Therefore, the reported time scales here represent those involved in preparation of motor response based on cerebellar learning and are more consistent with what has been reported in the literature in connection to tasks that require working memory (Howe et al, 2013;Kunimatsu et al, 2018;Soon et al, 2008;Tetzlaff et al, 2012), rather than what has been associated with motor control (Buhusi and Meck, 2005).…”

“…Studies on decision making however have been mainly focused on rodents or primates in which, due to technical limitations, recording of neuroactivity at high spatial and temporal resolution during decision making tasks can only be performed in parts of the brain, typically within the cortex (Gold and Shadlen, 2007;Murakami and Mainen, 2015;Svoboda and Li, 2018). Nevertheless, a hallmark of motor planning, the preparatory neuroactivity, has also been reported in different subcortical areas (Guo et al, 2017;Horwitz and Newsome, 1999;Kunimatsu et al, 2018;Liu et al, 2013;Svoboda and Li, 2018).…”

“…While the above findings in the cortex have provided some insights into the neuronal basis underlying action selection and the relationship between preparatory neuroactivity and motor response, several observations point towards the importance of taking a brain-wide approach to decision making that also includes subcortical regions and their interactions with the cortex (Cisek and Kalaska, 2010;Gao et al, 2018;Guo et al, 2017;Horwitz and Newsome, 1999;Kunimatsu et al, 2018;Liu et al, 2013). Support for this notion comes also from the fact that decision making almost inevitably requires access to or can be modulated by brain functions such as short-term memory, internal states or reward expectation that are known to have a sub-cortical representation (Abbott et al, 2017;Allen et al, 2017).…”

Cerebellar contribution to preparatory activity in motor neocortex

“…We found no difference in the effect of unilateral vs bilateral PC photoactivation on type 1 (n 226 = 10, 8 inhibited, 3 mice), type 2 (n = 13, 10 inhibited) or type 3 ALM neurons (n = 33, 18 inhibited, 11 227 excited; Figure S10B), except for shorter latency of inhibition upon unilateral photoactivation (8 ms vs 14 228 ms for unilateral photoactivation; Figure S10C). These data suggest that other brain regions involved in 229 motor preparation such as the basal ganglia (Kunimatsu et al, 2018), may contribute to the recovery of 230 preparatory activity. 231…”

“…information re-establishes cerebello-cortical activity once this circuit recovers. The basal ganglia have 380 also been shown to process preparatory activity(Kunimatsu et al, 2018;Ohmae et al, 2017) and might 381 therefore contribute a separate subcortical signal for motor preparation. 382Given that multiple closed-loop circuits have been identified between the subdivisions of 383 cerebellum and the neocortex(Habas et al, 2009;Kelly and Strick, 2003;Middleton and Strick, 1997; 384 Proville et al, 2014;Ramnani, 2006) we suggest that ALM and the lateral crus 1-DN cerebellar pathway 385 constitutes one such circuit dedicated to the generation of precisely-timed preparatory activity.…”