Organization of Corollary Discharge Neurons in Monkey Medial Dorsal Thalamus

Abstract

A corollary discharge (CD) is a copy of a neuronal command for movement sent to other brain regions to inform them of the impending movement. In monkeys, a circuit from superior colliculus (SC) through medial-dorsal nucleus of the thalamus (MD) to frontal eye field (FEF) carries such a CD for saccadic eye movements. This circuit provides the clearest example of such internal monitoring reaching cerebral cortex. In this report we first investigated the functional organization of the critical MD relay by systematically recording neurons within a grid of penetrations. In two male rhesus macaque monkeys (Macaca mulatta), we found that lateral MD neurons carrying CD signals discharged before saccades to ipsilateral as well as contralateral visual fields instead of just contralateral fields, often had activity over large movement fields, and had activity from both central and peripheral visual fields. Each of these characteristics has been found in FEF, but these findings indicate that these characteristics are already present in the thalamus. These characteristics show that the MD thalamic relay is not passive but instead assembles inputs from the SC before transmission to cortex. We next determined the exact location of the saccade-related CD neurons using the grid of penetrations. The neurons occupy an anterior-posterior band at the lateral edge of MD, and we established this band in stereotaxic coordinates to facilitate future study of CD neurons. These observations reveal both the organizational features of the internal CD signals within the thalamus, and the location of the thalamic relay for those signals.

Visuomotor learning from postdictive motor error

“…It is also possible that plasticity occurs subcortically in MD thalamus. It was recently shown that MD thalamus is not a passive relay station but actively assembles SC inputs before CD information is transmitted to the FEF ( Cavanaugh et al, 2020 ).…”

“…The corollary discharge is assumed to be processed via several pathways. The most prominent pathway extends from superior colliculus (SC) via MD thalamus to the frontal eye fields (FEF; Sommer and Wurtz, 2002 ; Sommer and Wurtz, 2004a ; Sommer and Wurtz, 2004b ; Sommer and Wurtz, 2006 ; Cavanaugh et al, 2020 ). Other pathways extend from SC via the thalamic pulvinar to parietal and occipital cortex ( Wurtz et al, 2011 ; Berman et al, 2017 ), from the cerebellum via the ventrolateral thalamus to frontal cortex ( Middleton and Strick, 2000 ; Gaymard et al, 2001 ; Zimmermann et al, 2015 ) and back from FEF through the basal ganglia to SC ( Sommer and Wurtz, 2008 ; Wurtz, 2008 ).…”

Neural Substrates and Models of Omission Responses and Predictive Processes

“…A hypothetical overlap of the substrates of corollary discharges, sensory suppression, omission responses, and MMN can only be tested in animals. Such an investigation would also address the possibility that the omission responses observed in active protocols are not fully cortical: corollary discharges drive sensory suppression also in pre-cortical stations of the sensory pathway, such as the dorsal cochlear nucleus (Singla et al, 2017) and the thalamus (Cavanaugh et al, 2020). These stations have not yet been tested for omission responses.…”

The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses

“…The observed increased consistency in phase probably reflects the interaction of motor preparation and auditory stimuli, as the motor intention may facilitate the onset of auditory processing, especially for speech sounds. This facilitation could even be as early as in the subcortical pathway, as the studies in vision and eye movement suggest that the CD signals can be available in the colliculus and thalamus ( Cavanaugh et al, 2020 ).…”