A change in behavioral state switches the pattern of motor output that underlies rhythmic head and orofacial movements.

The breathing rhythm serves as a reference that paces orofacial motor actions and orchestrates active sensing. Past work has reported that pacing occurs solely at a fixed phase relative to sniffing. We re-evaluated this constraint as a function of exploratory behavior. Allocentric and egocentric rotations of the head and the electromyogenic activity of the motoneurons for head and orofacial movements were recorded in free-ranging rats as they searched for food. We found that a change in state from foraging to rearing is accompanied by a large phase shift in muscular activation relative to sniffing, and a concurrent change in the frequency of sniffing, so that pacing now occurs at one of the two phases. Further, head turning is biased such that an animal gathers a novel sample of its environment upon inhalation. In total, the coordination of active sensing has a previously unrealized computational complexity. This can emerge from hindbrain circuits with fixed architecture and credible synaptic time delays.

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.

Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat.

The delineation of sensorimotor circuits that guide exploration begins with an understanding of the pattern of motor outputs [1]. These motor patterns provide a clue to the form of the underlying circuits [2-4] (but see [5]). We focus on the behaviors that rodents use to explore their peripersonal space through goal-directed positioning of their nose, head, and vibrissae. Rodents sniff in response to novel odors, reward expectation, and as part of social interactions [6-12]. Sniffing serves olfaction [13, 14], while whisking synchronized to sniffing serves vibrissa-based touch [6, 15, 16]. We quantify the ethology of exploratory nose and head movements in relation to breathing. We find that sniffing is accompanied by prominent lateral and vertical deflections of the nose, i.e., twitches, which are driven by activation of the deflector nasi muscles [17]. On the timescale of individual breaths, nose motion is rhythmic and has a maximum deflection following the onset of inspiration. On a longer timescale, excursions of the nose persist for several breaths and are accompanied by an asymmetry in vibrissa positioning toward the same side of the face. Such directed deflections can be triggered by a lateralized source of odor. Lastly, bobbing of the head as the animal cranes and explores is phase-locked to sniffing and to movement of the nose. These data, along with prior results on the resetting of the whisk cycle at the onset of inspiration [15, 16, 18], reveal that the onset of each breath initiates a "snapshot" of the orofacial sensory environment. VIDEO ABSTRACT.