Two Psychophysical Channels of Whisker Deflection in Rats Align with Two Neuronal Classes of Primary Afferents

Abstract

The rat whisker system has evolved into in an excellent model system for sensory processing from the periphery to cortical stages. However, to elucidate how sensory processing finally relates to percepts, methods to assess psychophysical performance pertaining to precise stimulus kinematics are needed. Here, we present a head-fixed, behaving rat preparation that allowed us to measure detectability of a single whisker deflection as a function of amplitude and peak velocity. We found that velocity thresholds for detection of smallamplitude stimuli (Ͻ3°) were considerably higher than for detection of large-amplitude stimuli (Ͼ3°). This finding suggests the existence of two psychophysical channels mediating detection of whisker deflection: one channel exhibiting high amplitude and low velocity thresholds (W1), and the other channel exhibiting high velocity and low amplitude thresholds (W2). The correspondence of W1 to slowly adapting (SA) and W2 to rapidly adapting (RA) neuronal classes in the trigeminal ganglion was revealed in acute neurophysiological experiments. Neurometric plots of SA and RA cells were closely aligned to psychophysical performance in the corresponding W1 and W2 parameter ranges. Interestingly, neurometric data of SA cells fit the behavior best if it was based on a short time window integrating action potentials during the initial phasic response, in contrast to integrating across the tonic portion of the response. This suggests that detection performance in both channels is based on the assessment of very few spikes in their corresponding groups of primary afferents.

Rat Whisker Psychophysics

“…Few studies, however, have detailed the psychophysics of whisker-based tactile discriminations in behaving animals, and the biologically relevant parameters of whisker stimulation remain unknown. In a recent study in The Journal of Neuroscience, Stüttgen et al (2006) address these issues, revealing psychophysical detection thresholds of whisker deflections and their putative neural correlates in primary afferents.…”

“…Using awake, head-restrained rats, Stüttgen et al developed an operant conditioning task to determine the amplitude and velocity detection thresholds of precisely controlled whisker deflections [Stüttgen et al (2006) To initiate the delivery of a water reward, rats were trained to lick a water spout after detection of a whisker deflection. To keep rats "honest," Stütt-gen et al (2006) imposed a time-out penalty in the event of random licking and included "catch" trials without any stimulation.…”

“…With these procedural parameters in place, unsignaled lick responses were kept well below chance levels (12-18%). During testing, whisker deflections of varying amplitude (1-12°) and velocity (62-1500°/s) were presented and lick responses were recorded [Stüttgen et al (2006) Behavioral data were quantified by computing the probability of observing a lick response to a given whisker deflection. These data indicated that the detection of whisker deflections is determined by at least two kinematic parameters: amplitude and velocity.…”

“…These data indicated that the detection of whisker deflections is determined by at least two kinematic parameters: amplitude and velocity. Specifically, rats reliably detected low-velocity whisker deflections (Ͻ750°/s) of sufficiently high amplitude (Ͼ3°) [Stüttgen et al (2006), their In search of the neural substrates of W1 and W2, Stüttgen et al (2006) performed microelectrode recordings from the trigeminal ganglion (TG), the first station in the whisker-to-barrel pathway. The authors sampled from both slowly adapting (SA) and rapidly adapting (RA) neurons in the TG.…”

“…The authors sampled from both slowly adapting (SA) and rapidly adapting (RA) neurons in the TG. In response to the same stimulation parameters used during behavioral testing, RA neurons responded to all amplitudes of whisker stimulation when presented at high velocity (Ͼ750°/s) [Stüttgen et al (2006) [Stüttgen et al (2006), their Fig. 7 (http:// www.jneurosci.org/cgi/content/full/26/30/ 7933/F7)].…”