Whisking and sniffing are predominant aspects of exploratory behavior in rodents, yet the neural mechanisms that generate their motor patterns remain largely uncharacterized. We use anatomical, behavioral, electrophysiological, and pharmacological tools to demonstrate that these patterns are coordinated by respiratory centers in the ventral medulla. We delineate a distinct region in the ventral medulla that provides rhythmic input to the facial motoneurons that drive protraction of the vibrissae. Neuronal output from this region is reset at each inspiration by direct input from the preBötzinger complex, such that high frequency sniffing has a one-to-one coordination with whisking while basal respiration is accompanied by intervening whisks that occur between breaths. We conjecture that the respiratory nuclei, which project to other premotor regions for oral and facial control, function as a master clock for behaviors that coordinate with breathing.

SUMMARY 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.

Summary Animals employ active touch to optimize the acuity of their tactile sensors. Prior experimental results and models lead to the hypothesis that sensory inputs are used in a recurrent manner to tune the position of the sensors. A combination of electrophysiology, intersectional genetic viral labeling and manipulation, and classical tracing, allowed us to identify second-order sensorimotor loops that control vibrissa movements by rodents. Facial motoneurons that drive intrinsic muscles to protract the vibrissae receive a short latency inhibitory input, followed by synaptic excitation, from neurons located in the oralis division of the trigeminal sensory complex. In contrast, motoneurons that retract the mystacial pad, and indirectly retract the vibrissae, receive only excitatory input from interpolaris cells that further project to the thalamus. Silencing this feedback alters retraction. The observed pull-push circuit for motion control at the lowest-level sensorimotor loop provides a mechanism for the rapid modulation of vibrissa touch during exploration of peri-personal space.

In a number of mammals muscle dilator nasi (naris) is known as a muscle that reduces nasal airflow resistance by dilating the nostrils. Here we show that in rats the tendon of this muscle inserts into the aponeurosis above the nasal cartilage. Electrical stimulation of this muscle lifts the nose and deflects it sideway towards the side of stimulation, but does not change the size of the nares. In the head-fixed alert rat, electromyographic activity of muscle dilator nasi is tightly coupled to nose motion, not to opening of the nares. Yet, contraction of muscle dilator nasi occurs during the pre-inspiratory phase of the respiratory cycle, suggesting a role in sniffing and sampling odorants. We also show that opening of the nares results from contraction of pars maxillaris profunda of the muscle nasolabialis profundus. This muscle attaches to the outer wall of the nasal cartilage and to the plate of the mystacial pad. Contraction of this muscle exerts a dual action: it pulls the lateral nasal cartilage outwardly, thus dilating the naris, and it drags the plate of the mystacial pad rostralward, provoking a slight retraction of the whiskers. On the basis of these results, we propose that muscle dilator nasi of the rat be renamed muscle deflector nasi, and that pars maxillaris profunda of the muscle nasolabialis profundus be named muscle dilator nasi.

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