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• W2965852474 abstract "Preparatory activity is found across the motor network. In this issue of Neuron, Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar show that preparatory activity in the anterior lateral motor cortex (ALM) and cerebellum is related to the prediction of reward delivery and that the cerebellum provides a learned timing signal to the ALM. Preparatory activity is found across the motor network. In this issue of Neuron, Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar show that preparatory activity in the anterior lateral motor cortex (ALM) and cerebellum is related to the prediction of reward delivery and that the cerebellum provides a learned timing signal to the ALM. In day-to-day life, we are constantly conducting goal-directed movements, whether that be throwing a ball, reaching for a cup of coffee, or even typing on a keyboard, perfecting those movements is inherently rewarding. The cerebellum is thought to have a hand in this process, learning to time our actions by generating internal models—neural representations—of the body and its interaction with the world, predicting the sensory outcomes of an action, and comparing them with sensory input to refine future movements. The cerebellum can store multiple internal models and can select a model depending on the behavioral context required. Motor planning leading up to goal-directed movements has been found across the motor network. One such area in rodents is the anterior lateral motor neocortex (ALM), which may have functional similarities to the primate premotor cortex and is an area shown to be important for planning of voluntary movements (Guo et al., 2017Guo Z.V. Inagaki H.K. Daie K. Druckmann S. Gerfen C.R. Svoboda K. Maintenance of persistent activity in a frontal thalamocortical loop.Nature. 2017; 545: 181-186Crossref PubMed Scopus (251) Google Scholar). ALM neurons exhibit preparatory activity before movement, and maintenance of this activity is dependent on a bidirectional connection with the motor thalamus (Guo et al., 2017Guo Z.V. Inagaki H.K. Daie K. Druckmann S. Gerfen C.R. Svoboda K. Maintenance of persistent activity in a frontal thalamocortical loop.Nature. 2017; 545: 181-186Crossref PubMed Scopus (251) Google Scholar; Figure 1). The significance of this preparatory activity is not well understood but is thought to link past events with future movements (Guo et al., 2017Guo Z.V. Inagaki H.K. Daie K. Druckmann S. Gerfen C.R. Svoboda K. Maintenance of persistent activity in a frontal thalamocortical loop.Nature. 2017; 545: 181-186Crossref PubMed Scopus (251) Google Scholar). For example, when faced with the decision of “should I throw the ball to my friend using an over- or underarm technique” during a game of catch, our brains use a combination of sensory input (is my arm fatigued by our game of catch, how far away is my friend) and recent reward history (the last time I threw the ball to my friend they dropped a high throw) to help decide which action to take. The ALM may represent a key node in the motor network that is crucial in selecting motor actions. ALM projects to the cerebellum via the basal pontine nuclei, and the output of the cerebellum via the cerebellar nuclei projects to the motor thalamus (Figure 1), thereby allowing the two brain regions to form closed-circuit loops (Gao et al., 2018Gao Z. Davis C. Thomas A.M. Economo M.N. Abrego A.M. Svoboda K. De Zeeuw C.I. Li N. A cortico-cerebellar loop for motor planning.Nature. 2018; 563: 113-116Crossref PubMed Scopus (183) Google Scholar). How the ALM and cerebellum work cooperatively to ensure the success of a goal-orientated movement is unknown and is explored in this issue of Neuron by Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar. Combining behavior, optogenetics, and neural recordings, Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar recorded from the ALM and cerebellum of mice running in a virtual reality corridor. The mice learned to associate a visual cue with a reward delivered 40 cm farther along the virtual track. Preparatory activity was observed prior to reward delivery that precedes movement in a subset of ALM neurons and in the dentate nucleus (DN) of the cerebellum, as previously described by Guo et al., 2017Guo Z.V. Inagaki H.K. Daie K. Druckmann S. Gerfen C.R. Svoboda K. Maintenance of persistent activity in a frontal thalamocortical loop.Nature. 2017; 545: 181-186Crossref PubMed Scopus (251) Google Scholar and Gao et al., 2018Gao Z. Davis C. Thomas A.M. Economo M.N. Abrego A.M. Svoboda K. De Zeeuw C.I. Li N. A cortico-cerebellar loop for motor planning.Nature. 2018; 563: 113-116Crossref PubMed Scopus (183) Google Scholar. Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar then examined the influence of DN activity on ALM preparatory firing by manipulating inhibitory Purkinje cell (PC) input to the DN optogenetically alongside DN and ALM recordings (Figure 1). Photoactivating PCs in a region known to both receive visuomotor inputs and project to the DN for 1 s preceding the reward point inhibited DN activity and subsequently interrupted ALM preparatory activity. While the observation that activity in the DN precedes movement has been shown previously (e.g., Thach, 1975Thach W.T. Timing of activity in cerebellar dentate nucleus and cerebral motor cortex during prompt volitional movement.Brain Res. 1975; 88: 233-241Crossref PubMed Scopus (123) Google Scholar), the finding that this preparatory increase in both DN and ALM may be related to the timing of reward is novel, as the preparatory activity was only observed in the rewarded section of the virtual corridor, emerged prior to reward delivery, and was not related to running speed or licking events outside of the reward zone. Because the timing of the reward is dependent on how slowly or quickly the mice reach the reward following the visual cue for reward, Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar predicted that if preparatory activity is related to the timing of reward, then activity for slow trials should start earlier and, conversely, faster trials should start later. This is precisely what Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar were able to demonstrate. The study by Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar adds to a growing literature demonstrating that neural correlates related to reward are signaled within the cerebellum (Wagner et al., 2017Wagner M.J. Kim T.H. Savall J. Schnitzer M.J. Luo L. Cerebellar granule cells encode the expectation of reward.Nature. 2017; 544: 96-100Crossref PubMed Scopus (260) Google Scholar, Heffley et al., 2018Heffley W. Song E.Y. Xu Z. Taylor B.N. Hughes M.A. McKinney A. Joshua M. Hull C. Coordinated cerebellar climbing fiber activity signals learned sensorimotor predictions.Nat. Neurosci. 2018; 21: 1431-1441Crossref PubMed Scopus (77) Google Scholar, Kostadinov et al., 2019Kostadinov D. Beau M. Pozo M.B. Häusser M. Predictive and reactive reward signals conveyed by climbing fiber inputs to cerebellar Purkinje cells.Nat. Neurosci. 2019; 22: 950-962Crossref Scopus (84) Google Scholar). PCs receive inputs via two major pathways: climbing fiber (CF) inputs from the inferior olive (IO) and mossy fiber (MF) inputs via granule cells (GrC), which are thought to carry sensory and motor information from the neocortex and periphery (Figure 1). Reward anticipatory activity has been recorded in GrCs (Wagner et al., 2017Wagner M.J. Kim T.H. Savall J. Schnitzer M.J. Luo L. Cerebellar granule cells encode the expectation of reward.Nature. 2017; 544: 96-100Crossref PubMed Scopus (260) Google Scholar). CFs are thought to provide a teaching signal to PCs that is used to update internal models in motor learning. CFs trigger complex spikes in PCs; Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar examined the CF-to-PC response by using the presence of so called “fat spikes” in their cerebellar recordings as a proxy for CF activity and found an increase in the frequency of fat spikes at reward delivery. This is consistent with recent work by Heffley et al., 2018Heffley W. Song E.Y. Xu Z. Taylor B.N. Hughes M.A. McKinney A. Joshua M. Hull C. Coordinated cerebellar climbing fiber activity signals learned sensorimotor predictions.Nat. Neurosci. 2018; 21: 1431-1441Crossref PubMed Scopus (77) Google Scholar and Kostadinov et al., 2019Kostadinov D. Beau M. Pozo M.B. Häusser M. Predictive and reactive reward signals conveyed by climbing fiber inputs to cerebellar Purkinje cells.Nat. Neurosci. 2019; 22: 950-962Crossref Scopus (84) Google Scholar, in which the authors both observed CF activity associated with reward expectation and delivery arranged in a topographical manner within the forelimb controlling areas of the cerebellum. Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar suggest that the cortico-ponto-cerebellar pathway relays relevant visual and motor activity from the neocortex to combine with reward prediction signals from the GrCs. Learning in the cerebellum is often attributed to plasticity at parallel fiber (PF)-to-PC synapses under the control of CF signals. Thus, the CFs that provide reward timing signals may refine the timing of preparatory activity at the PF-to-PC synapse. Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar concluded that after having learned to predict upcoming rewards, cerebellar output via the DN contributes to the precise timing of preparatory signals in the ALM to refine goal-directed movement. An alternative hypothesis that could be considered is that the cerebellum provides a signal related to the success or failure of the chosen internal model via the DN output. This is then relayed to the ALM via the motor thalamus to shape decisions on future goal-directed movements. Outstanding questions follow this study and those that recently have shown that the cerebellum is involved in the signaling of reward. (1) Are dopamine neurons involved in the association between reward and a goal-directed movement? Although dopaminergic projections to the basal ganglia and dopamine-dependent reinforcement learning based on reward prediction errors are well known (Schultz et al., 2017Schultz W. Stauffer W.R. Lak A. The phasic dopamine signal maturing: from reward via behavioural activation to formal economic utility.Curr. Opin. Neurobiol. 2017; 43: 139-148Crossref PubMed Scopus (98) Google Scholar), dopaminergic projections have been shown to project to the cerebellar cortex (Ikai et al., 1992Ikai Y. Takada M. Shinonaga Y. Mizuno N. Dopaminergic and non-dopaminergic neurons in the ventral tegmental area of the rat project, respectively, to the cerebellar cortex and deep cerebellar nuclei.Neuroscience. 1992; 51: 719-728Crossref PubMed Scopus (164) Google Scholar) and the cerebellar nuclei are known to project to midbrain dopaminergic neurons (Carta et al., 2019Carta I. Chen C.H. Schott A.L. Dorizan S. Khodakhah K. Cerebellar modulation of the reward circuitry and social behavior.Science. 2019; 363: 6424Crossref Scopus (239) Google Scholar). Viral and optogenetic strategies targeting dopaminergic inputs to the cerebellum during reward-based task would shed light on this question. (2) How does preparatory activity in the ALM and DN develop as the mice learn to associate the cue and reward? Recordings from both brain regions throughout learning may help explain how preparatory activity is acquired and over what timescale. (3) Is preparatory activity related to reward found in other areas of the cerebellum, or is it unique to the parts of the cerebellum now thought to be involved in higher cognitive functions? (4) If the signal from the DN reflects a timing signal, how will this affect behavior? Addressing this would be pertinent as a lack of behavioral effect was evident when inactivating the DN with photoactivation of the overlying PCs in the tasks used by Chabrol et al., 2019Chabrol F.P. Blot A. Mrsic-Flogel T.D. Cerebellar contribution to preparatory activity in motor neocortex.Neuron. 2019; 103 (this issue): 506-519Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar and by Gao et al., 2018Gao Z. Davis C. Thomas A.M. Economo M.N. Abrego A.M. Svoboda K. De Zeeuw C.I. Li N. A cortico-cerebellar loop for motor planning.Nature. 2018; 563: 113-116Crossref PubMed Scopus (183) Google Scholar, who found no behavioral deficits in a sensory discrimination task. Regardless of the outstanding questions, the findings are an important step toward understanding how motor networks interact to contribute to the preparatory activity related to precise timing of goal-directed behaviors and reward. Cerebellar Contribution to Preparatory Activity in Motor NeocortexChabrol et al.NeuronJune 11, 2019In BriefChabrol et al. show that the cerebellum is directly involved in maintaining preparatory activity in the premotor neocortex during learned, goal-directed behavior. Their results suggest the cerebellum provides a learned timing signal required for motor preparation in the neocortex. Full-Text PDF Open Access" @default.
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• W2965852474 title "Timing Rewarding Movements" @default.
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