UC San Diego

Breathing, one of the fundamental and indispensable rhythms of life, has been proposed to serve as a “master clock” that binds the orofacial sensory inputs in rodents (Welker, 1964; Kleinfeld et al., 2014). Previous studies showed whisking (Moore et al., 2013; Deschênes et al., 2016), nose twitching (Kurnikova et al., 2017), and head-bobbing (Kurnikova et al., 2017) are one-to-one phase-locked to breathing as the rat explores its peri-personal space in a head-fixed setting or on a small and confined platform.In this work, we test this “breathing primacy hypothesis” (Kleinfeld et al., 2014) on the foraging behavior in rats, where the orofacial motor actions may become more complex as the rat has a larger field to explore. First, we delineate the motor control of the horizontal head movement in the allocentric and egocentric coordinates. We show the coordination with breathing is bimodal and depends on the postural states. We record the electromyogram (EMG) from neck muscles and find their activities phase-locked to breathing at distinct phases, suggesting that the breathing rhythm is involved in hierarchical motor control. We explore the dimension along the behavioral repertoire and observe that the phase relationship between the neck muscles and breathing shifts as the rat switches between the foraging and rearing states, accompanied by a change in the sniffing rate. We use models of weakly coupled phase oscillators (Kuramoto, 1984; Kopell and Ermentrout, 1986; Kopell, 1988; Schuster and Wagner, 1989; Ermentrout and Kleinfeld, 2001; Kleinfeld and Mehta, 2006) to explain the experimental results and show that the rat can pattern the motor outputs differently by driving the neck oscillator with different breathing frequencies. Lastly, we delineate the differential coordination of whisking and nose twitching with breathing in the foraging and rearing modes. Together with the insights in the heading control, our work suggests that the fixed connectivity among the brainstem oscillators can generate variable programs of motor outputs to fulfill different behavioral goals.