Vibrissa sensation in superior colliculus: wide-field sensitivity and state-dependent cortical feedback

Rodents use their vibrissae (whiskers) to sense and navigate the environment. A main target of this sensory information is the superior colliculus in the midbrain, which rats can use to detect meaningful whisker stimuli in behavioral contexts. Here, we used field potential, single-unit, and intracellular recordings to show that, although cells in the intermediate layers of the superior colliculus respond relatively effectively to single whiskers, the cells respond much more robustly to simultaneous, or nearly simultaneous, wide-field (multiwhisker) stimuli. The enhanced multiwhisker response is temporally stereotyped, consisting of two short latency peaks caused by convergent trigeminal synaptic inputs and cortical feedback, respectively. The cells are highly sensitive to the degree of temporal dispersion and contact order of multiwhisker stimuli, which makes them excellent detectors of initial multiwhisker contact. In addition, their output is most robust during quiescent states because of the dependence of cortical feedback on forebrain activation, and this may serve as an alerting signal to drive orienting responses.