Effects of Optogenetic Activation of Corticothalamic Terminals in the Motor Thalamus of Awake Monkeys

• Type of Material: Article
• Authors: Adriana Galvan, Emory University; Xing Hu, Emory University; Yoland Smith, Emory University; Thomas Wichmann, Emory University
• Language: English
• Date: 2016-03-23
• Publisher: Society for Neuroscience
• Publication Version: Final Published Version
• Copyright Statement: © 2016 the authors.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1523/JNEUROSCI.4363-15.2016
• Title of Journal or Parent Work: Journal of Neuroscience
• ISSN: 0270-6474
• Volume: 36
• Issue: 12
• Start Page: 3519
• End Page: 3530
• Grant/Funding Information: This work was supported by the National Institutes of Health (NIH)/Office of Research Infrastructure Programs (Grant P51-OD011132 to the Yerkes National Primate Research Center), NIH/National Institute of Neurological Disorders and Stroke (NINDS Udall Center Grant P50-NS071669 and Grant GR01-NS083386 to T.W.).
• Keywords: motor cortex; SUBTHALAMIC NUCLEUS; MACACA-MULATTA THALAMUS; Neurosciences & Neurology; BASAL GANGLIA; RETICULAR NUCLEUS; C1V1; optogenetics; SUPPLEMENTARY MOTOR; Science & Technology; GLOBUS-PALLIDUS; ChR2; single unit recording; RELAY NUCLEI; Life Sciences & Biomedicine; motor thalamus; Neurosciences; CORTICAL AREAS
• Research Categories: Health Sciences, General; Biology, Neuroscience

Abstract

The role of the corticothalamic projection in the ventral motor thalamus remains poorly understood. Therefore, we studied the electrophysiological responses of neurons in the basal ganglia and cerebellar receiving-territories of the motor thalamus (BGMT and CbMT, respectively) using optogenetic activation of corticothalamic projections in awake rhesus macaques. After injections of viral vectors carrying the excitatory opsins ChR2 or C1V1 into the primary motor and premotor cortices of two monkeys, we used optrodes to light activate opsin-expressing neurons in cortex or their terminals in the thalamus while simultaneously recording the extracellular activity of neuronsin the vicinity of the stimulationsites. Asexpected, light activation of opsinsin the cerebral cortex evoked robust,short-latency increases in firing of cortical neurons. In contrast, light stimulation of corticothalamic terminals induced small-amplitude, long-latency increases and/or decreases of activity in thalamic neurons. In postmortemmaterial, opsins were found to be expressed in cell bodies and dendrites of cortical neurons and along their corticothalamic projections. At the electron microscopic level, opsin labeling was confined to unmyelinated preterminal axons and small terminals that formed asymmetric synapses with dendrites of projection neurons or GABAergic interneurons in BGMT and CbMT and with neurons in the reticular thalamic nucleus. The morphological features of the transfected terminals, along with the long latency and complex physiological responses of thalamic neurons to their activation, suggest a modulatory role of corticothalamic afferents upon the primate ventral motor thalamus.