Motor directional tuning across brain areas: directional resonance and the role of inhibition for directional accuracy

Margaret Y Mahan,Apostolos P Georgopoulos

doi:10.3389/fncir.2013.00092

Abstract

Motor directional tuning (Georgopoulos et al., 1982) has been found in every brain area in which it has been sought for during the past 30-odd years. It is typically broad, with widely distributed preferred directions and a population signal that predicts accurately the direction of an upcoming reaching movement or isometric force pulse (Georgopoulos et al., 1992). What is the basis for such ubiquitous directional tuning? How does the tuning come about? What are the implications of directional tuning for understanding the brain mechanisms of movement in space? This review addresses these questions in the light of accumulated knowledge in various sub-fields of neuroscience and motor behavior. It is argued (a) that direction in space encompasses many aspects, from vision to muscles, (b) that there is a directional congruence among the central representations of these distributed “directions” arising from rough but orderly topographic connectivities among brain areas, (c) that broad directional tuning is the result of broad excitation limited by recurrent and non-recurrent (i.e., direct) inhibition within the preferred direction loci in brain areas, and (d) that the width of the directional tuning curve, modulated by local inhibitory mechanisms, is a parameter that determines the accuracy of the directional command.

Highlights

As in the thalamus and cortex, the conclusion is unavoidable: either there is an amazing degree of selectivity in the innervation of single neurons by afferent fibers or inhibitory and other synaptic mechanisms ensure that most inputs remain subthreshold (Jones, 2007, p. 164)In the quote above, Ted Jones referred to the high density of innervation of dorsal column nuclei by fibers traveling along the medial lemniscus, in what he called “enormous morphological convergence at all levels of the ascending somatosensory pathways” (Jones, 2007, p. 164), between periphery and cortex
The difference lies in the content of information, which is manifested as a receptive field in the somatosensory cortex (Mountcastle et al, 1957) and as a directional tuning field in the motor cortex (Georgopoulos and Stefanis, 2007)
Motor directional tuning correspondence would interconnect directional tuning fields across various motor areas, which would account for the concurrent activation of these areas at the initiation and execution of a movement in a particular direction

Summary

NEURAL CIRCUITS

This review addresses these questions in the light of accumulated knowledge in various sub-fields of neuroscience and motor behavior It is argued (a) that direction in space encompasses many aspects, from vision to muscles, (b) that there is a directional congruence among the central representations of these distributed “directions” arising from rough but orderly topographic connectivities among brain areas, (c) that broad directional tuning is the result of broad excitation limited by recurrent and non-recurrent (i.e., direct) inhibition within the preferred direction loci in brain areas, and (d) that the width of the directional tuning curve, modulated by local inhibitory mechanisms, is a parameter that determines the accuracy of the directional command

INTRODUCTION

Mahan and Georgopoulos

Deep cerebellar nuclei Yes