A Cellular Mechanism for the Transformation of a Sensory Input into a Motor Command

TLDR

The initiation and control of locomotion depend on processing sensory inputs, and lamprey reticulospinal (RS) neurons—key descending elements of the locomotor system—have been extensively studied to understand this cellular basis. Ca(2+) imaging and intracellular recordings were employed to examine how RS neurons are activated by cutaneous stimulation. Pressure on the skin elicited a linear input/output in RS neurons until a threshold, after which a Ca(2+)-dependent depolarizing plateau—mediated by a Ca(2+)-activated nonselective cation current, blocked by NMDA receptor antagonists or BAPTA—was generated, linking the sensory stimulus to a motor command that initiates swimming.

Abstract

The initiation and control of locomotion largely depend on processing of sensory inputs. The cellular bases of locomotion have been extensively studied in lampreys where reticulospinal (RS) neurons constitute the main descending system activating and controlling the spinal locomotor networks. Ca(2+) imaging and intracellular recordings were used to study the pattern of activation of RS neurons in response to cutaneous stimulation. Pressure applied to the skin evoked a linear input/output relationship in RS neurons until a threshold level, at which a depolarizing plateau was induced, the occurrence of which was associated with the onset of swimming activity in a semi-intact preparation. The occurrence of a depolarizing plateau was abolished by blocking the NMDA receptors that are located on RS cells. Moreover, the depolarizing plateaus were accompanied by a rise in [Ca(2+)](i), and an intracellular injection of the Ca(2+) chelator BAPTA into single RS cells abolished the plateaus, suggesting that the latter are Ca(2+) dependent and rely on intrinsic properties of RS cells. The plateaus were shown to result from the activation of a Ca(2+)-activated nonselective cation current that maintains the cell in a depolarized state. It is concluded that this intrinsic property of the RS neuron is then responsible for the transformation of an incoming sensory signal into a motor command that is then forwarded to the spinal locomotor networks.