Contrasting modulatory effects from the dorsal and ventral premotor cortex on primary motor cortex outputs

  1. Numa Dancause1,2
  1. 1Département de Neurosciences, Faculté de Médecine, Université de Montréal, Québec, Canada, H3C 3J7
  2. 2Groupe de recherche sur le système nerveux central (GRSNC), Université de Montréal, Québec, Canada, H3C 3J7
  1. Corresponding author: Numa Dancause, PT, PhD, Groupe de recherche sur le système nerveux central (GRSNC), Département de Neurosciences, Université de Montréal, C.P. 6128 succursale Centre-ville, H2C 3J7, Phone: 514-343-6317, email: numa.dancause{at}umontreal.ca
  1. Author contributions: S.l.C., S.Q., and N.D. analyzed data; S.l.C. and N.D. wrote the paper; A.H., S.Q., and N.D. performed research; N.D. designed research.

Abstract

The dorsal and ventral premotor cortices (PMd and PMv) each take part in unique aspects for the planning and execution of hand movements. These premotor areas are components of complex anatomical networks that include the primary motor cortex (M1) of both hemispheres. One way PMd and PMv could play distinct roles for hand movements is by differently modulating the outputs of M1. Yet, patterns of effects from PMd and PMv on the outputs of M1 have not been systematically compared. Our goals were to study how PMd within the same (i.e. ipsilateral or iPMd) and in the opposite hemisphere (i.e. contralateral or cPMd) can shape M1 outputs and compare these effects to those induced by PMv. We used paired-pulse protocols with intracortical microstimulation techniques in sedated female cebus monkeys while recording electromyographic (EMG) signals from intrinsic hand and forearm muscles. A conditioning stimulus was delivered in iPMd or cPMd concurrently or prior to a test stimulus in M1. The patterns of modulatory effects from PMd were compared to those from PMv collected in the same animals. Striking differences were revealed. Conditioning stimulation in iPMd induced more frequent and powerful inhibitory effects on M1 outputs in comparison to iPMv. In the opposite hemisphere, cPMd conditioning induced more frequent and powerful facilitatory effects than cPMv. These contrasting patterns of modulatory effects could allow PMd and PMv to play distinct functions for the control of hand movements and predispose them to undertake different, perhaps somewhat opposite roles in motor recovery after brain injury.

Significance statement:

The dorsal and ventral premotor cortices (PMd and PMv) are two specialized areas involved in the control of hand movements in primates. One way PMd and PMv can participate in hand movements is by modulating or shaping the primary motor cortex (M1) outputs to hand muscles. Here, we studied the patterns of modulation from PMd, within the same and in the opposite hemisphere, on the outputs of M1 and compared them to those from PMv. We found that PMd and PMv have strikingly different effects on M1 outputs. These contrasting patterns of modulation provide a substrate that may allow PMd and PMv to carry distinct functions for the preparation and execution of hand movements, and for recovery after brain injury.

Footnotes

  • The authors declare no conflict of interest.

  • This work was supported by a Natural Sciences and Engineering Research Council of Canada discovery grant to ND (NSERC; RGPIN-2016-05718). SLC was supported by a Master's salary award from NSERC. AH was supported by a postdoctoral fellowship by the GRSNC. We thank Kelsey N. Dancause for editing comments on the manuscript. The authors declare no competing financial interests.

  • Received February 16, 2017.
  • Revision received April 22, 2017.
  • Accepted May 9, 2017.