Thalamic input to motor cortex facilitates goal-directed action initiation

Abstract

Prompt execution of planned motor action is essential for survival. The interactions between frontal cortical circuits and the basal ganglia are central to goal-oriented action selection and initiation.1Graybiel A.M. The basal ganglia.Curr. Biol. 2000; 10: R509-R511Abstract Full Text Full Text PDF PubMed Scopus (391) Google Scholar, 2Hikosaka O. Nakamura K. Sakai K. Nakahara H. Central mechanisms of motor skill learning.Curr. Opin. Neurobiol. 2002; 12: 217-222Crossref PubMed Scopus (664) Google Scholar, 3Middleton F.A. Strick P.L. Basal ganglia and cerebellar loops: motor and cognitive circuits.Brain Res. Brain Res. Rev. 2000; 31: 236-250Crossref PubMed Scopus (1409) Google Scholar, 4Parent A. Hazrati L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop.Brain Res. Brain Res. Rev. 1995; 20: 91-127Crossref PubMed Scopus (1754) Google Scholar In rodents, the ventromedial thalamic nucleus (VM) is one of the critical nodes that conveys the output of the basal ganglia to the frontal cortical areas including the anterior lateral motor cortex (ALM).5Bosch-Bouju C. Hyland B.I. Parr-Brownlie L.C. Motor thalamus integration of cortical, cerebellar and basal ganglia information: implications for normal and parkinsonian conditions.Front. Comput. Neurosci. 2013; 7: 163Crossref PubMed Scopus (125) Google Scholar, 6Guo K. Yamawaki N. Svoboda K. Shepherd G.M.G. Anterolateral Motor Cortex Connects with a Medial Subdivision of Ventromedial Thalamus through Cell Type-Specific Circuits, Forming an Excitatory Thalamo-Cortico-Thalamic Loop via Layer 1 Apical Tuft Dendrites of Layer 5B Pyramidal Tract Type Neurons.J. Neurosci. 2018; 38: 8787-8797Crossref PubMed Scopus (24) Google Scholar, 7Kuramoto E. Fujiyama F. Nakamura K.C. Tanaka Y. Hioki H. Kaneko T. Complementary distribution of glutamatergic cerebellar and GABAergic basal ganglia afferents to the rat motor thalamic nuclei.Eur. J. Neurosci. 2011; 33: 95-109Crossref PubMed Scopus (70) Google Scholar, 8Sieveritz B. García-Muñoz M. Arbuthnott G.W. Thalamic afferents to prefrontal cortices from ventral motor nuclei in decision-making.Eur. J. Neurosci. 2019; 49: 646-657Crossref PubMed Scopus (15) Google Scholar, 9Tanaka Y.H. Tanaka Y.R. Kondo M. Terada S.I. Kawaguchi Y. Matsuzaki M. Thalamocortical Axonal Activity in Motor Cortex Exhibits Layer-Specific Dynamics during Motor Learning.Neuron. 2018; 100: 244-258.e12Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar Recent studies showed the critical role of ALM and its interplay with the motor thalamus in preparing sensory-cued rewarded movements, specifically licking.10Guo 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 (210) Google Scholar, 11Li N. Chen T.W. Guo Z.V. Gerfen C.R. Svoboda K. A motor cortex circuit for motor planning and movement.Nature. 2015; 519: 51-56Crossref PubMed Scopus (254) Google Scholar, 12Guo Z.V. Li N. Huber D. Ophir E. Gutnisky D. Ting J.T. Feng G. Svoboda K. Flow of cortical activity underlying a tactile decision in mice.Neuron. 2014; 81: 179-194Abstract Full Text Full Text PDF PubMed Scopus (318) Google Scholar Work in primates suggests that the basal ganglia output to the motor thalamus transmits an urgency or vigor signal,13Cisek P. Puskas G.A. El-Murr S. Decisions in changing conditions: the urgency-gating model.J. Neurosci. 2009; 29: 11560-11571Crossref PubMed Scopus (243) Google Scholar, 14Thura D. Cisek P. The Basal Ganglia Do Not Select Reach Targets but Control the Urgency of Commitment.Neuron. 2017; 95: 1160-1170.e5Abstract Full Text Full Text PDF PubMed Scopus (69) Google Scholar, 15Turner R.S. Desmurget M. Basal ganglia contributions to motor control: a vigorous tutor.Curr. Opin. Neurobiol. 2010; 20: 704-716Crossref PubMed Scopus (241) Google Scholar which leads to shortened reaction times and faster movement initiation. As yet, little is known about what signals are transmitted from the motor thalamus to the cortex during cued movements and how these signals contribute to movement initiation. In the present study, we employed a tactile-cued licking task in mice while monitoring reaction times of the initial lick. We found that inactivation of ALM delayed the initiation of cued licking. Two-photon Ca2+ imaging of VM axons revealed that the majority of the axon terminals in ALM were transiently active during licking. Their activity was predictive of the time of the first lick. Chemogenetic and optogenetic manipulation of VM axons in ALM indicated that VM inputs facilitate the initiation of cue-triggered and impulsive licking in trained mice. Our results suggest that VM thalamocortical inputs increase the probability and vigor of initiating planned motor responses.

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