High- and low-level computations for coordination of orofacial motor actions

Overall - Abstract
High- and low-level computations for coordination of orofacial motor actions
Neuronal circuits in the brainstem integrate control of life-sustaining motor actions, such as breathing and
feeding, with exploratory motor actions, such as sniffing, licking, nose and head turning, and, for rodents,
whisking. All of these contain a rhythmic component that is entrained by the breathing cycle. What are the
underlying circuits that produce these motor actions and how are they coordinated into flexible behaviors? Our
hypothesis is that high-level rhythmic signals use feedback to modulate the phase of low-level oscillator activity
on a cycle-wise basis. High-level broadband signals also regulate set-point and posture of effectors. Together,
low- and high-level signals lead to coordinated and precise rhythmic behaviors to achieve sensory goals.
We address our hypothesis using two theoretical concepts and a plethora of experimental procedures. One
theoretical concept is control theory. This concept emphasizes internal models, that is, computations that yield
signals to drive a physical plant, such as the vibrissae or the tongue, that respect the innervation of the
musculature. Control theory also emphasizes the role of feedback signals to correct the timing of rhythmic
actions. The second theoretical concept is coupled oscillators circuits, one for each rhythmic action with an
overall "coordinator". These guide schemes for the continual adjustment rhythmic action phases to form a precise
behavior. Theoretical guidance was pivotal toward the discovery of the oscillator for whisking, identify a
mechanism brain used to create a hierarchy of oscillators, and identifying modularity in the control of movement.
We seek to discover a second fundamental oscillator in the brainstem, one that controls chewing and licking.
In parallel, we will complete a biomechanical model of the tongue that includes changes in shape and turgidity
based on motor innervation of the muscles and the control of blood flow by local parasympathetic neurons.
Together with whisking and joint vibrissa and head movement, these are a trifecta of targets for high-level control.
A novel concept in our proposal is the fine control of rhythmic motion by high-level feedback to refine the
relative timing of different rhythm motor actions. Thus head position, tongue position, possibly whisker position
are optimized in the context of a behavior. We address this possibility through three interdependent approaches:
anatomical tracing of molecularly identified high-level cell types to molecularly identified low-level targets in the
medulla; recording and perturbing signals in superior colliculus that influence head orientation and whisking; and
recording and perturbing cortical signals that influence licking.
The collective expertise of our Team bridges state-of-the-art anatomical, behavioral, computational,
molecular, and physiological technologies. We have historically adhered to the highest standards in
experimentation, analysis, and theory. Critically, we are joined by top trainees in a diverse workforce committed
to progress on motor control, and we are dedicated to educating our trainees in a culture of curiosity and
scholastic excellence.