Behavioral state dependency of neural activity and sensory (whisker) responses in superior colliculus

Rats use their vibrissa (whiskers) to explore and navigate the environment. These sensory signals are distributed within the brain stem by the trigeminal complex and are also relayed to the superior colliculus in the midbrain and to the thalamus (and subsequently barrel cortex) in the forebrain. In the intermediate layers of the superior colliculus, whisker-evoked responses are driven by direct inputs from the trigeminal complex (trigeminotectal) and feedback from the barrel cortex (corticotectal). But the effects of the behavioral state of the animal on the spontaneous firing and sensory responses of these neurons are unknown. By recording from freely behaving rats, we show that the spontaneous firing of whisker sensitive neurons in superior colliculus is higher, or in an activated mode, during active exploration and paradoxical sleep and much lower, or in a quiescent/deactivated mode, during awake immobility and slow-wave sleep. Sensory evoked responses in superior colliculus also depend on behavioral state. Most notably, feedback corticotectal responses are significantly larger during the quiescent/deactivated mode, which tracks the barrel cortex responses on which they depend. Finally, sensory evoked responses depend not only on the state of the animal but also on the orienting response elicited by the stimulus, which agrees with the well known role of the superior colliculus in orienting about salient stimuli.