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. 2001 Jul 15;21(14):5374-80.
doi: 10.1523/JNEUROSCI.21-14-05374.2001.

Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator

P Gao  1 , R Bermejo, H P Zeigler
Affiliations

Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator

P Gao et al. J Neurosci. .

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.

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Figures

Fig. 1.
Fig. 1.
A, Schematic diagram of the optoelectronic monitoring system, indicating the position of the laser emitter and detector with respect to the head-fixed animal. In these experiments, all whiskers were intact on both sides of the face, and the right and left C-1 whiskers were marked for monitoring. For clarity, only a single set of emitters and detectors and only a single whisker are shown on one side of the face. B, Schematic diagram illustrating both the basic principle of the monitoring system and the process by which whisker displacements are transformed from CCD units to angular whisker positions. Thick black linesindicate the successive positions of the marked vibrissa during a whisking movement.
Fig. 2.
Fig. 2.
Whisking movement trajectories (angular position and time) for the right and left C-1 whiskers in a head-fixed animal recorded during the first test session. An 8.5 sec sample plotted at a lower resolution (every 10th data point) is shown at thetop. The shaded portion of the record highlights an 850 msec (cursor-selected) sample that is displayed at higher temporal resolution at the bottom. Upward and downward movements represent whisker protractions and retractions, respectively. The arrows labeled a,b, and c at the bottomidentify critical points (start, peak, and end, respectively) of the whisker movement that are extracted for kinematic analysis.
Fig. 3.
Fig. 3.
Kinematics of whisking behavior. A, Frequency distribution of whisking (i.e., protraction) amplitudes.B, Relative contributions of protraction and retraction to the total duration (movement time) of individual whisking movements. Data are for a single animal. C, Comparison of protraction (Pro) and retraction (Re) velocities during whisking. D, Comparison of protraction amplitudes in the right and left whiskers.
Fig. 4.
Fig. 4.
Amplitude scaling of protraction movements: relative contributions of protraction velocity and rise time variables. Plots are based on 100 randomly selected whisks from a single representative animal. Left, Relationship between protraction amplitude and peak velocity. Right, Relationship between protraction amplitude and rise time to peak protraction amplitude.
Fig. 5.
Fig. 5.
Whisking rhythmicity: plots of Fourier power spectra of whisking movements obtained from two representative animals.
Fig. 6.
Fig. 6.
Bilateral coordination of whisking movements on the two sides of the face: data for two representative animals.A, Frequency distribution of time differences between amplitude peaks in the right and left C-1 whiskers. B, Cross-correlograms of phase relationships among whisking movements on the right and left sides of the face.
Fig. 7.
Fig. 7.
Effects of repeated exposure to the test situation. Within-session (left) and between-session (right) changes in the amount and persistence of whisking activity as measured by the duration of individual whisking bouts.
Fig. 8.
Fig. 8.
Deafferentation of the whiskers does not significantly impact either protraction amplitude (left) or protraction velocity (right). Data are averages of each of the groups. Intact, Preoperative (n = 4); Uni-IOx, after unilateral sectioning of the infraorbital nerve (n = 5);Bi-IOx, after bilateral sectioning of the infraorbital nerve (n = 3).
Fig. 9.
Fig. 9.
Effects of trigeminal deafferentation on whisking patterns. Low-resolution plots of whisking movements recorded preoperatively (top), after unilateral infraorbital nerve sectioning (middle), and after sectioning of the remaining infraorbital nerve (bottom) are shown. For clarity, only the record of a whisker on one side of the face is shown, but increases in whisking frequency after unilateral deafferentation were seen in both right and left C-1 whiskers.
Fig. 10.
Fig. 10.
Trigeminal deafferentation and whisking rhythmicity. Plots of Fourier power spectra before and after sham (left), sequentially (middle), and during the first and third sessions (S1 and S3, respectively) after a one-stage bilateral deafferentation of the whiskers (right). For clarity, only data for a single whisker are presented, although effects were similar in both whiskers.
Fig. 11.
Fig. 11.
Whisker deafferentation and the bilateral coordination of whisking. A, Effects of bilateral deafferentation. Frequency distributions of time differences between amplitude peaks in the right and left C-1 whiskers before (top) and after (bottom) bilateral infraorbital sectioning performed in a single stage. The data shown in the graph represent group means for the three animals.B, Cross-correlograms of whisking movements on the right and left sides of the animal before (top) and after (bottom) unilateral infraorbital nerve sectioning. Peak shifts in the second and third components reflect the increased whisking frequency. Data are for a single representative animal.
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