Differential distribution of corticospinal projections from individual cytoarchitectonic fields in the monkey

Converging interactions between ascending proprioceptive afferents and descending corticospinal tract projections are critical in the modulation and coordination of skilled motor behaviors. Fundamental to these processes are the functional inputs and the mechanisms of integration in the brain and spinal cord between proprioceptive and corticospinal tract information. In this review, we first highlight key connections between corticospinal tract motor circuit and spinal interneurons that receive proprioceptive inputs. We will also address corticospinal tract access to the presynaptic inhibitory system in the spinal cord and its role in modulating proprioceptive stimuli. Lastly, we will focus on the corticospinal neuron influences on the dorsal column nuclei complex, an integration hub for processing ascending somatosensory information.

Proprioception is commonly described as the sense of body position and movement. However, an underappreciated aspect of this “hidden sixth sense” is how intimately it is tied to the systems that execute movement. Loss of proprioception devastates our ability to move; without the ability to replace it, a motor brain-computer interface cannot be expected to function well. Proprioceptive receptors, located mostly within the muscles and joints, signal limb state that is the consequence of descending motor commands to the muscles and their interaction with the effects of external forces. As proprioceptive afferents ascend the neuroaxis, they contribute to reflexes and muscle coordination before reaching the brainstem and thalamus, subject to descending modulatory influence from both the brainstem and sensorimotor cortex at all levels. Within the somatosensory cortex, area 3a, with its largely muscle-receptor inputs, shares many common features with the adjacent motor cortex and is certainly intimately involved in movement execution. The higher level representation that results from combination with cutaneous inputs in area 2 likely provides critical limb state information to the posterior parietal cortex for use in movement planning. Proprioceptive signals are also involved in internal model formation and error calculation in the cerebellum, where deficits share many features in common with those experienced following deafferentation. The challenge of developing a proprioceptive brain interface is certainly a technical one, but also one of reaching a deeper understanding of all the systems—and their interconnectedness—outlined in this chapter.

Little is known about the organizational and functional connectivity of the corticospinal (CS) circuits that are essential for voluntary movement. Here, we map the connectivity between CS neurons in the forelimb motor and sensory cortices and various spinal interneurons, demonstrating that distinct CS-interneuron circuits control specific aspects of skilled movements. CS fibers originating in the mouse motor cortex directly synapse onto premotor interneurons, including those expressing Chx10. Lesions of the motor cortex or silencing of spinal Chx10⁺ interneurons produces deficits in skilled reaching. In contrast, CS neurons in the sensory cortex do not synapse directly onto premotor interneurons, and they preferentially connect to Vglut3⁺ spinal interneurons. Lesions to the sensory cortex or inhibition of Vglut3⁺ interneurons cause deficits in food pellet release movements in goal-oriented tasks. These findings reveal that CS neurons in the motor and sensory cortices differentially control skilled movements through distinct CS-spinal interneuron circuits.