Volitional inspiration is mediated by two independent output channels in the primary motor cortex

Abstract

AbstractThe diaphragm is a multifunctional muscle that mediates both autonomic and volitional inspiration. It is critically involved in vocalization, postural stability, and expulsive core–trunk functions, such as coughing, hiccups, and vomiting. In macaque monkeys, we used retrograde transneuronal transport of rabies virus injected into the left hemidiaphragm to identify cortical neurons that have multisynaptic connections with phrenic motoneurons. Our research demonstrates that representation of the diaphragm in the primary motor cortex (M1) is split into two spatially separate and independent sites. No cortico–cortical connections are known to exist between these two sites. One site is located dorsal to the arm representation within the central sulcus and the second site is lateral to the arm. The dual representation of the diaphragm warrants a revision to the somatotopic map of M1. The dorsal diaphragm representation overlaps with trunk and axial musculature. It is ideally situated to coordinate with these muscles during volitional inspiration and in producing intra‐abdominal pressure gradients. The lateral site overlaps the origin of M1 projections to a laryngeal muscle, the cricothyroid. This observation suggests that the coordinated control of laryngeal muscles and the diaphragm during vocalization may be achieved, in part, by co‐localization of their representations in M1. The neural organization of the two diaphragm sites underlies a new perspective for interpreting functional imaging studies of respiration and/or vocalization. Furthermore, our results provide novel evidence supporting the concept that overlapping output channels within M1 are a prerequisite for the formation of muscle synergies underlying fine motor control.