Attention Robustly Gates a Closed-Loop Touch Reflex

Rats' large whiskers (macrovibrissae) are used to explore their nearby environment, typically using repetitive protraction-retraction "whisking" motions that are coordinated with head and body movements [1-8]. Once objects are detected, the rat can further explore the object tactually by using both the macrovibrissae and an array of shorter, stationary microvibrissae on the chin, as well as by using the lips [9-11]. When touch occurs during whisking, a fast reflexive response, termed a touch-induced pump (TIP), may be triggered. During a TIP, the whisker slightly retracts and protracts again, doubling the number of pressure onsets per contact. In head-fixed rats, TIPs occur in ∼25% of the contacts [12]. Here we report that the occurrence of TIPs depends strongly on attention, indicated by head-turning toward an object: when rats intended to explore an object, either after encountering it during free exploration or when expecting its existence, the probability of a TIP increased from <30% to >65% without an increase in TIP latency. TIP regulation was unilateral and specific to the attended object; when two objects were palpated bilaterally simultaneously, TIP probability increased to >65% and decreased to <20% for contacts with the apparently-attended and apparently-unattended object, respectively. A data-driven computational model indicates that attentional gating could not be triggered by object contact, due to temporal constraints; rather, it could be based on a normally enabled or whisking-triggered scheme. Taken together, our results suggest that object-related attention regulates contact dynamics by gating the operation of a brainstem motor-sensory-motor loop and that this regulation is optimized for fast reaction.