Corticospinal Inputs to Primate Motoneurons Innervating the Forelimb from Two Divisions of Primary Motor Cortex and Area 3a

Abstract

Previous anatomical work in primates has suggested that only corticospinal axons originating in caudal primary motor cortex ("new M1") and area 3a make monosynaptic cortico-motoneuronal connections with limb motoneurons. By contrast, the more rostral "old M1" is proposed to control motoneurons disynaptically via spinal interneurons. In six macaque monkeys, we examined the effects from focal stimulation within old and new M1 and area 3a on 135 antidromically identified motoneurons projecting to the upper limb. EPSPs with segmental latency shorter than 1.2 ms were classified as definitively monosynaptic; these were seen only after stimulation within new M1 or at the new M1/3a border (incidence 6.6% and 1.3%, respectively; total n ϭ 27). However, most responses had longer latencies. Using measures of the response facilitation after a second stimulus compared with the first, and the reduction in response latency after a third stimulus compared with the first, we classified these late responses as likely mediated by either long-latency monosynaptic (n ϭ 108) or non-monosynaptic linkages (n ϭ 108). Both old and new M1 generated putative long-latency monosynaptic and non-monosynaptic effects; the majority of responses from area 3a were non-monosynaptic. Both types of responses from new M1 had significantly greater amplitude than those from old M1. We suggest that slowly conducting corticospinal fibers from old M1 generate weak late monosynaptic effects in motoneurons. These may represent a stage in control of primate motoneurons by the cortex intermediate between disynaptic output via an interposed interneuron seen in nonprimates and the fast direct monosynaptic connections present in new M1.

Corticocortical Systems Underlying High-Order Motor Control

“…This function could be particularly relevant to allow these phylogenetically older structures to store and perform new motor skills. As an example, the "new M1" (Rathelot and Strick, 2009), with its privileged access to spinal motoneurons (Witham et al, 2016), the evolution of parietal areas related to hand functions (Padberg et al, 2007), and an expanded parietofrontal system (Caminiti et al, 2015) can be considered as crucial evolutionary enrichments for motor functions and cognition. Within this frame, the direct parietospinal projection (Rathelot et al, 2017;Innocenti et al, 2019) can convey to the motor output command signals (Mountcastle, 1978), as well as information relevant to other functions, such as visuomotor adaptation, that after rapid error correction return behavior to baseline performance (Shmuelof and Krakauer, 2011) and probably occurs in the parietoponto-cerebellar system.…”

Slowly-conducting pyramidal tract neurons in macaque and rat

“…If there were a general relationship between PTN soma size and axon diameter (Sakai and Woody 1988), then it is interesting to note that some of the layer V corticospinal neurons that were transneuronally labelled by (Rathelot and Strick 2006) had very small soma diameters, hinting that some slow PTNs could make direct, cortico-motoneuronal connections. Monosynaptic effects from these PTNs would be expected to have late onsets, and such effects have been reported (Maier et al 1998;Witham et al 2016).…”

Kinnier Wilson’s puzzling features of amyotrophic lateral sclerosis

“…Corticomotoneuronal connections from fast-conducting CST fibres arise exclusively from the caudal primary motor cortex (new M1) and its border with 3a. But the more rostral primary motor cortex (old M1), also has corticomotoneuronal connections through more slowly conducting CST axons and through di-synaptic connections with motoneurons via interposed interneurons 45. At the spinal level, the CST terminates in the ventral horns but also sends connexions into the dorsal spinal cord, traditionally viewed as the ‘sensory’ horn.…”