The activity of primary motor cortex corticospinal neurons during tool use by macaque monkeys

It has been suggested that the distinctive capacity of some nonhuman primates to use tools may reflect a well-developed corticospinal system and, in particular, direct cortico-motoneuronal (CM) connections to hand muscles. We investigated the activity of corticospinal neurons in the primary motor cortex hand area during the use of a tool by two adult macaque monkeys. They used a light rake to retrieve food rewards placed in their extrapersonal space. An analysis of EMG activity showed that the rake task involved a complex interaction of muscles acting on the digits, hand, and arm. Sixty-nine corticospinal neurons were identified antidromically as pyramidal tract neurons (PTNs). When tested on the rake task, most (64 of 69; 93%) showed a significant modulation of their discharge during at least one of three task periods: grasping the rake, projecting it beyond the food reward, and then pulling it back to retrieve the reward. Discharge patterns were heterogeneous, and many PTNs showed significant suppression of discharge during raking. Seventeen of the 69 PTNs recorded during the rake task were further identified as CM cells, exerting clear postspike facilitation on digit muscles, demonstrating that the CM system contributes to the skilled use of tools. We compared the activity of each PTN on the rake task with that during precision grip. Most PTNs (90%) modulated their activity significantly for both tasks, demonstrating that PTNs activated by a task involving fractionated movements of the digits are also recruited during rake use, although there were often contrasting patterns of PTN recruitment and muscle activity for the two tasks.