Bidirectional control of orienting behavior by the substantia nigra pars reticulata: distinct significance of head and whisker movements

Abstract

Detection of an unexpected, novel, or salient stimulus typically leads to an orienting response by which animals move the head, in concert with the sensors (e.g., eyes, pinna, whiskers), to evaluate the stimulus. The basal ganglia are known to control orienting movements through tonically active GABAergic neurons in the substantia nigra pars reticulata (SNr) that project to the superior colliculus. Using optogenetics, we explored the ability of GABAergic SNr neurons on one side of the brain to generate orienting movements. In a strain of mice that express channelrhodopsin (ChR2) in both SNr GABAergic neurons and afferent fibers, we found that continuous blue light produced a robust sustained excitation of SNr neurons which generated ipsiversive orienting. Conversely, in the same animal, trains of blue light excited afferent fibers more effectively than continuous blue light, producing a robust sustained inhibition of SNr neurons which generated contraversive orienting. When ChR2 expression was restricted to either GABAergic SNr neurons or GABAergic afferent fibers from the striatum, blue light patterns in SNr produced only ipsiversive or contraversive orienting movements, respectively. Interestingly, whisker positioning and the reaction to an air-puff on the whiskers were incongruent between SNr-evoked ipsiversive and contraversive head movements, indicating that orienting driven by exciting or inhibiting SNr neurons have different behavioral significance. In conclusion, unilateral SNr neuron excitation and inhibition produce orienting movements in opposite directions and, apparently, with distinct behavioral significance.

Significance Statement

The substantia nigra pars reticulata (SNr) is the main output nucleus of the basal ganglia in the midbrain and is known to be involved in orienting behavior. We found a way to bidirectionally control the firing of SNr cells in same animal. This approach revealed that excitation or inhibition of these cells controlled the direction of orienting head movements in opposite directions and, apparently, with different behavioral significance.