The role of kinematic events in whisker-related tactile perception

Abstract

Rodents use active whisker movements to explore their environment. The physical parameters of vibrissa deflections, which carry the texture information and are used by the tactile system for discrimination, are unknown. Particularly, it remains unclear whether perception relies on parameters such as frequency (e.g., spectral information) and intensity (e.g., mean speed) which need to be integrated over time or whether it has access to instantaneous kinematic parameters (i.e., the details of the trajectory). The search for instantaneous kinematic parameters is motivated by findings from studies on rodent vibrissae biomechanics showing that short-lived kinematic events, abrupt movements called ‘slips’, carry texture information and could therefore be used for tactile perception. Here, I use a novel detection of change paradigm in head-fixed rats, which presents passive vibrissa stimuli in seamless sequence for discrimination. Unlike previous paradigms, this procedure ensures that processes of decision making do not need to rely on memory functions and can, instead, directly tap into sensory signals. In a first attempt, repetitive pulsatile stimuli were employed in a noise free environment to optimally control the parameter space. I find that discrimination performance based on instantaneous kinematic cues far exceeds the ones provided by frequency and intensity. Neuronal modeling based on barrel cortex single-unit activity shows that small populations of sensitive neurons provide a transient signal that optimally fits the characteristic of the subject’s perception. However, a realistic scenario involves background noise (e.g. evoked by rubbing across the texture) and kinematic ‘slip’ events, carrying texture information. Therefore, if these events are used for tactile perception, the neuronal system would need to differentiate slip-evoked spikes from those evoked by noise. To test the animals under these more realistic conditions, I presented passive whisker-deflections, consisting of ‘slip-like’ events (waveforms mimicking ‘slips’ occurring with real textures) embedded into background noise. Varying the event shape (ramp or pulse), kinematics (amplitude, velocity, etc.), and the probability of occurrence, I observed that rats could readily detect ‘slip-like’ events of different shapes against a noisy background. Psychophysical curves revealed that larger events improved performance while increased probability of occurrence had barely any effect. These results strongly support the notion that encoding of instantaneous ‘slip’ kinematics dominantly determines whisker-related tactile perception while the computation of time integrated parameters plays a minor role.