Low- and high-level coordination of orofacial motor actions.

Orofacial motor actions are movements that, in rodents, involve whisking of the vibrissa, deflection of the nose, licking and lapping with the tongue, and consumption through chewing. These actions, along with bobbing and turning of the head, coordinate to subserve exploration while not conflicting with life-supporting actions such as breathing and swallowing. Orofacial and head movements are comprised of two additive components: a rhythm that can be entrained by the breathing oscillator and a broadband component that directs the actuator to the region of interest. We focus on coordinating the rhythmic component of actions into a behavior. We hypothesize that the precise timing of each constituent action is continually adjusted through the merging of low-level oscillator input with sensory-derived, high-level rhythmic feedback. Supporting evidence is discussed.

Interchangeable Role of Motor Cortex and Reafference for the Stable Execution of an Orofacial Action.

Animals interact with their environment through mechanically active, mobile sensors. The efficient use of these sensory organs implies the ability to track their position; otherwise, perceptual stability or prehension would be profoundly impeded. The nervous system may keep track of the position of a sensorimotor organ via two complementary feedback mechanisms-peripheral reafference (external, sensory feedback) and efference copy (internal feedback). Yet, the potential contributions of these mechanisms remain largely unexplored. By training male rats to place one of their vibrissae within a predetermined angular range without contact, a task that depends on knowledge of vibrissa position relative to their face, we found that peripheral reafference is not required. The presence of motor cortex is not required either, except in the absence of peripheral reafference to maintain motor stability. Finally, the red nucleus, which receives descending inputs from motor cortex and cerebellum and projects to facial motoneurons, is critically involved in the execution of the vibrissa positioning task. All told, our results point toward the existence of an internal model that requires either peripheral reafference or motor cortex to optimally drive voluntary motion.SIGNIFICANCE STATEMENT How does an animal know where a mechanically active, mobile sensor lies relative to its body? We address this basic question in sensorimotor integration using the motion of the vibrissae in rats. We show that rats can learn to reliably position their vibrissae in the absence of sensory feedback or in the absence of motor cortex. Yet, when both sensory feedback and motor cortex are absent, motor precision is degraded. This suggests the existence of an internal model able to operate in closed- and open-loop modes, requiring either motor cortex or sensory feedback to maintain motor stability.

A vibrissa pathway that activates the limbic system.

Vibrissa sensory inputs play a central role in driving rodent behavior. These inputs transit through the sensory trigeminal nuclei, which give rise to the ascending lemniscal and paralemniscal pathways. While lemniscal projections are somatotopically mapped from brainstem to cortex, those of the paralemniscal pathway are more widely distributed. Yet the extent and topography of paralemniscal projections are unknown, along with the potential role of these projections in controlling behavior. Here, we used viral tracers to map paralemniscal projections. We find that this pathway broadcasts vibrissa-based sensory signals to brainstem regions that are involved in the regulation of autonomic functions and to forebrain regions that are involved in the expression of emotional reactions. We further provide evidence that GABAergic cells of the Kölliker-Fuse nucleus gate trigeminal sensory input in the paralemniscal pathway via a mechanism of presynaptic or extrasynaptic inhibition.

Circuits in the Ventral Medulla That Phase-Lock Motoneurons for Coordinated Sniffing and Whisking.

The exploratory behavior of rodents is characterized by stereotypical movements of the vibrissae, nose, and head, which are phase locked with rapid respiration, that is, sniffing. Here we review the brainstem circuitry that coordinates these actions and propose that respiration may act as a master clock for binding orofacial inputs across different sensory modalities.

Inhibition, Not Excitation, Drives Rhythmic Whisking.

Sniffing and whisking typify the exploratory behavior of rodents. These actions involve separate oscillators in the medulla, located respectively in the pre-Bötzinger complex (preBötC) and the vibrissa-related region of the intermediate reticular formation (vIRt). We examine how these oscillators synergize to control sniffing and whisking. We find that the vIRt contains glycinergic/GABAergic cells that rhythmically inhibit vibrissa facial motoneurons. As a basis for the entrainment of whisking by breathing, but not vice versa, we provide evidence for unidirectional connections from the preBötC to the vIRt. The preBötC further contributes to the control of the mystacial pad. Lastly, we show that bilateral synchrony of whisking relies on the respiratory rhythm, consistent with commissural connections between preBötC cells. These data yield a putative circuit in which the preBötC acts as a master clock for the synchronization of vibrissa, pad, and snout movements, as well as for the bilateral synchronization of whisking.