Multiple Modes of Phase Locking between Sniffing and Whisking during Active Exploration

Abstract

Sense organs are often actively controlled by motor processes and such active sensing profoundly shapes the timing of sensory information flow. The temporal coordination between different active sensing processes is less well understood but is essential for multisensory integration, coordination between brain regions, and energetically optimal sampling strategies. Here we studied the coordination between sniffing and whisking, the motor processes in rodents that control the acquisition of smell and touch information, respectively. Sniffing, high frequency respiratory bouts, and whisking, rapid back and forth movements of mystacial whiskers, occur in the same theta frequency range (4-12 Hz) leading to a hypothesis that these sensorimotor rhythms are phase-locked. To test this, we monitored sniffing using a thermocouple in the nasal cavity and whisking with an electromyogram (EMG) of the mystacial pad in rats engaged in an open field reward foraging behavior. During bouts of exploration, sniffing and whisking showed strong one-to-one phase-locking within the theta frequency range (4-12 Hz). Interestingly, we also observed multi-mode phase-locking with multiple whisks within a sniff cycle or multiple sniffs within a whisk cycle – always at the same preferred phase. This specific phase relationship coupled the acquisition phases of the two sensorimotor rhythms, inhalation and whisker protraction. Our results suggest that sniffing and whisking may be under the control of interdependent rhythm generators that dynamically coordinate active acquisition of olfactory and somatosensory information.

The Brainstem Oscillator for Whisking and the Case for Breathing as the Master Clock for Orofacial Motor Actions

“…Concurrent measurements of breathing and whisking in head-restrained rats reveal key aspects of their coordination (Moore and Deschênes et al 2013; Ranade et al 2013), and extend Welker’s initial descriptions (Fig. 3).…”

How the brainstem controls orofacial behaviors comprised of rhythmic actions

“…These behaviors involve the use of common muscles in the snout 4, 17 , and their robust one-to-one coordination suggested that they might depend on a common rhythm generator. Since Welker’s initial qualitative observations, synchronous sniffing and whisking has been more completely described 18, 19 and quantified 20, 21 in a number of subsequent studies in rats. There is also evidence that high-frequency sniffing and whisking are phase locked in mice 20 ; however, one study reports a lack of such coordination in this species 22 .…”

Inhibition, Not Excitation, Drives Rhythmic Whisking

“…This proximity is likely to be functionally relevant since whisking is tightly coupled to fast breathing, typically called sniffing. Yet even fast whisking is gated separately from breathing (Welker, 1964; Moore et al, 2013; Ranade et al, 2013). The vibrissa-related region of the IRt (vIRt) contains facial premotor neurons and neurons that fire either in phase or in antiphase with vibrissa protraction.…”