Superior colliculus cells sensitive to active touch and texture during whisking

Abstract

Rats sense the environment through rhythmic vibrissa protractions, called active whisking, which can be simulated in anesthetized rats by electrically stimulating the facial motor nerve. Using this method, we investigated barrel cortex field potential and superior colliculus single-unit responses during passive touch, whisking movement, active touch, and texture discrimination. Similar to passive touch, whisking movement is signaled during the onset of the whisker protraction by short-latency responses in barrel cortex that drive corticotectal responses in superior colliculus, and all these responses show robust adaptation with increases in whisking frequency. Active touch and texture are signaled by longer latency responses, first in superior colliculus during the rising phase of the protraction, likely driven by trigeminotectal inputs, and later in barrel cortex by the falling phase of the protraction. Thus, superior colliculus is part of a broader vibrissa neural network that can decode whisking movement, active touch, and texture.

The search space of the rat during whisking behavior

“…The centering of the vibrissal tips about the eyes may represent a peripheral correlate of the neural registration of the tactile and visual systems found in structures such as the superior colliculus (McHaffie and Stein, 1982;Dauvergne et al, 2004;Bezdudnaya and Castro-Alamancos, 2011). This geometric arrangement will inherently tend to ensure that tactile and visual modalities operate within the same coordinate system and bring tactile and visual maps into registration.…”

Modulation of artificial whisking related signals in barrel cortex

“…Note that the evoked responses are strongly suppressed by frequency, reflecting robust rapid sensory adaptation. Note also that in a previous study (Bezdudnaya and Castro-Alamancos 2011) puff responses evoked in barrel cortex were smaller than artificial whisking responses, but in that case the puff was centered on the receptive field of cells recorded in superior colliculus. In the present study, puff responses are typically larger than artificial whisking responses because the puff is centered on the receptive field of the barrel cortex recordings.…”

“…Artificial whisking was conducted as previously described (Bezdudnaya and Castro-Alamancos 2011). To trigger artificial whisking, we cut and positioned a pair of stainless steel wires in the buccal branch of the facial nerve (0.7-1 mm apart) and delivered a train of five pulses (100-s duration) at 100 Hz.…”

“…The stimulus intensity was adjusted (0.04-to 0.17-mA range) to produce a protraction with a 10 -35°a ngle. In a few cases, we used synchronous video monitoring (500 frames per second; Motionscope, Red Lake Imaging, Morgan Hill, CA) to track whisker movement frame by frame (Bezdudnaya and Castro-Alamancos 2011). After tracking of each frame, the movements measured during each of the last 30 trains were averaged.…”

“…In fact, population neural responses driven by artificial whisking have a characteristic large amplitude response to the onset of the whisking protraction, we call peakA (for simplicity), which is followed by a much smaller response during the offset of the protraction (retraction), called peakB (Bezdudnaya and Castro-Alamancos 2011). Interestingly, the cortical response evoked by the retraction, peakB, is enhanced by active touch compared with whisking in air (Bezdudnaya and Castro-Alamancos 2011;Derdikman et al 2006;Yu et al 2013). Here we further explored the nature of this retraction signal.…”