Patterns of cortical input to the primary motor area in the marmoset monkey

Abstract

In primates the primary motor cortex (M1) forms a topographic map of the body, whereby neurons in the medial part of this area control movements involving trunk and hindlimb muscles, those in the intermediate part control movements involving forelimb muscles, and those in the lateral part control movements of facial and other head muscles. This topography is accompanied by changes in cytoarchitectural characteristics, raising the question of whether the anatomical connections also vary between different parts of M1. To address this issue, we compared the patterns of cortical afferents revealed by retrograde tracer injections in different locations within M1 of marmoset monkeys. We found that the entire extent of this area is unified by projections from the dorsocaudal and medial subdivisions of premotor cortex (areas 6DC and 6M), from somatosensory areas 3a, 3b, 1/2, and S2, and from posterior parietal area PE. While cingulate areas projected to all subdivisions, they preferentially targeted the medial part of M1. Conversely, the ventral premotor areas were preferentially connected with the lateral part of M1. Smaller but consistent inputs originated in frontal area 6DR, ventral posterior parietal cortex, the retroinsular cortex, and area TPt. Connections with intraparietal, prefrontal, and temporal areas were very sparse, and variable. Our results demonstrate that M1 is unified by a consistent pattern of major connections, but also shows regional variations in terms of minor inputs. These differences likely reflect requirements for control of voluntary movement involving different body parts.

Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited

“…Thus, some of the false positives identified in the present analysis could possibly be true positives; as a result, the specificity of all tractography techniques would be underestimated. However, studies that used retrograde tracers in the macaque (51) and other primates (52,53) have found that the cortico-cortical and corticothalamic regions identified as being directly connected to the injection sites PCG and V4v tend to be bidirectional. Moreover, our own results suggest that this aspect does not contribute to a large bias in the rate of false positives.…”

The cortical motor system of the marmoset monkey (Callithrix jacchus)

“…In particular, based on mediolateral variations in the size of layer 5 pyramidal neurons, marmoset M1 is composed of 3 architectural divisions (Burman et al, 2008(Burman et al, , 2014a; fields 4a/b and 4c of Paxinos et al, 2012), similar to that of other primates (Watanabe-Sawaguchi et al, 1991).…”

“…2, left) originate in medial (6M) and caudal premotor areas (6DC and 6V), whereas areas 6DR and 8C contribute sparser inputs (Burman et al, 2014a); connections of M1 with premotor areas are reciprocal (Burman Table 1). To some extent, variations in the exact composition of inputs to different parts of M1 also reflect its topographic organization, with specific emphases on connections to the regions of head, forelimb and trunk/hindlimb musculature representations (Burman et al, 2014a).…”

“…The medial fields of the anterior cingulate cortex are likely to provide cognitive, emotional, and motivational influences on motor function (Vogt et al, 1992;Devinsky et al, 1995;Shima and Tanji, 1998;Kuwabara et al, 2014), through divergent projections to sensorimotor, prefrontal, and limbic areas. Tentative homologies between parts of area 24 and the motor fields have been proposed in the marmoset (Burman et al, 2014a), largely based on the somatotopy of connections; however, physiological evidence is still lacking.…”

Differential modulation of motor network connectivity during movements of the upper and lower limbs

“…The role of premotor input onto M1 560 Premotor areas feature cortical representations of both the upper 561 and lower limb, which are highly interconnected with M1 as well as spi-562 nal motor neurons (Burman et al, 2014;Dum and Strick, 2005;Shimazu 563 et al, 2004). Hence, from an anatomical perspective, premotor areas are 564 likely to be involved in the coordination of movements of the hands and 565 feet alike.…”