Whisker Deafferentation and Rodent Whisking Patterns: Behavioral Evidence for a Central Pattern Generator

Abstract

Even in the absence of explicit stimulation, rats emit patterns of rhythmic whisking movements. Because of their stereotyped nature and their persistence after sensory denervation and cortical ablation, whisking movements have been assumed to reflect the output of a central pattern generator (CPG). However, identification of a movement pattern as the product of a CPG requires evidence that its generation, patterning, and coordination are independent of sensory input. To provide such evidence, we used optoelectronic instrumentation to obtain high-resolution records of the movement trajectories of individual whiskers in rats whose heads were fixed to isolate their exploratory whisking from exafferent inputs. Unconditioned whisking patterns were quantitatively characterized by a biometric analysis of the kinematics, rhythmicity, and coordination of bilaterally homologous vibrissa movements. Unilateral and bilateral sectioning of the infraorbital nerve, which innervates the whiskers, was then performed to block reafferent inputs generated by the animal's own whisking movements. Unilateral sectioning of the nerve has no effect on whisking kinematics but is followed by a significant but relatively transient bilateral increase in whisking frequency. However, bilateral deafferentation, when performed in a single-stage procedure, does not disrupt the generation, patterning, or bilateral coordination of whisking patterns in the rat. These findings provide strong behavioral evidence for a whisking CPG and are discussed in relation to its possible location and properties.

Biomechanics of the Vibrissa Motor Plant in Rat: Rhythmic Whisking Consists of Triphasic Neuromuscular Activity

“…Moreover, the effect of whisking frequency on the pattern of muscle activity is of critical importance for characterizing the hypothetical central pattern generator(s) that underlie whisking (Welker, 1964;Semba and Komisaruk, 1984;Gao et al, 2001;Berg and Kleinfeld, 2003;Hattox et al, 2003;Cramer and Keller, 2006). Previously, m. nasolabialis was shown to activate at a constant phase lag with respect to the intrinsic muscles even as the frequency of whisking varied .…”

“…As such, this procedure has enabled other difficult behavioral tasks (Gao et al, 2001;Bermejo et al, 2002;Gao et al, 2003b;Friedman et al, 2006) and intracellular (Crochet and Petersen, 2006) and extracellular (Sachdev et al, 2000;Kleinfeld et al, 2002;Melzer et al, 2006) recording studies. Yet it has been heretofore undocumented how head restraint may alter whisking behavior.…”

“…Lesion studies have shown that whisking persists after sensory nerve transection (Welker, 1964;Gao et al, 2001;Berg and Kleinfeld, 2003;Berg et al, 2006), contralateral motor cortex ablation (Gao et al, 2003b), and extensive decerebration (Welker, 1964). These results argue for a brainstem central pattern generator to drive rhythmic whisking.…”

“…Trained animals typically whisk for bouts of 1 s or more during which the vibrissae move predominantly in the horizontal plane (Bermejo et al, 2002) with great temporal regularity . Rhythmic whisking exhibits bilateral symmetry (Gao et al, 2001) in the absence of head movements (Towal and Hartmann, 2006) or contact with an object (Sachdev et al, 2003;Mitchinson et al, 2007). Thus, whisking may be described by a small number of possibly interdependent control parameters, which include frequency of whisking as well as amplitude and anteroposterior set point of both vibrissa and pad motion.…”

Spatiotemporal Characteristics of Neuronal Sensory Integration in the Barrel Cortex of the Rat

“…In natural conditions, rats perform whisking at frequencies from 2 to 20 Hz (Carvell and Simons 1990;Gao et al 2001;Welker 1964). Thus the low-frequency stimulation (typically 0.5 Hz) usually applied in experiments reflects the state the rat is in while resting.…”