Abolition of lemniscal barrellette patterning in Prrxl1 knockout mice: Effects upon ingestive behavior.

Ingestive behaviors in mice are dependent on orosensory cues transmitted via the trigeminal nerve, as confirmed by transection studies. However, these studies cannot differentiate between deficits caused by the loss of the lemniscal pathway vs. the parallel paralemniscal pathway. The paired-like homeodomain protein Prrxl1 is expressed widely in the brain and spinal cord, including the trigeminal system. A knockout of Prrxl1 abolishes somatotopic barrellette patterning in the lemniscal brainstem nucleus, but not in the parallel paralemniscal nucleus. Null animals are significantly smaller than littermates by postnatal day 5, but reach developmental landmarks at appropriate times, and survive to adulthood on liquid diet. A careful analysis of infant and adult ingestive behavior reveals subtle impairments in suckling, increases in time spent feeding and the duration of feeding bouts, feeding during inappropriate times of the day, and difficulties in the mechanics of feeding. During liquid diet feeding, null mice display abnormal behaviors including extensive use of the paws to move food into the mouth, submerging the snout in the diet, changes in licking, and also have difficulty consuming solid chow pellets. We suggest that our Prrxl1(-/-) animal is a valuable model system for examining the genetic assembly and functional role of trigeminal lemniscal circuits in the normal control of eating in mammals and for understanding feeding abnormalities in humans resulting from the abnormal development of these circuits.

Vibrissae motor cortex unit activity during whisking.

Rats generate stereotyped exploratory (5-12 Hz) vibrissa movements when navigating through their environment. Like other rhythmic behaviors, the production of whisking relies on a subcortical pattern generator. However, the relatively large vibrissae representation in motor cortex (vMCx) suggests that cortex also contributes to the control of whisker movements. The goal of this study was to examine the relationship between neuronal activity in vMCx and the kinematics of vibrissae movements. We recorded multiunit activity (MUA) and single units in the rhythmic region of vMCx while measuring vibrissa position in awake, head-restrained rats. The rats were engaged in one of two behavioral tasks where they were rewarded for either 1) producing noncontact whisking epochs that met specified criteria (epochs ≥4 Hz, whisks >5 mm) or 2) whisking to contact an object. There was significant coherence between the frequency of MUA and vibrissae movements during free-air whisking but not when animals were using their vibrissae to contact an object. Spike rate in vMCx was most frequently correlated with the amplitude of vibrissa movements; correlations with movement frequency did not exceed chance levels. These findings suggest that the specific parameter under cortical control may be the amplitude of whisker movements.

Wally Welker and neurobehavioral evolution: an appreciation and bibliography.

The following review and appreciation of the pioneering work and character of Wallace I. (Wally) Welker provides a historical perspective on Welker's life-long quest for answers to fundamental questions on the relationships among brain, behavior, and evolution, and evaluates his impact upon comparative behavioral neuroscience.

Functional assessments of the rodent facial nerve: a synkinesis model.

OBJECTIVES/HYPOTHESIS: Rodent whisker movement has been used as a tool, after facial nerve manipulation, to quantify functional recovery. We have recently established a method to study functional correlates of aberrant regeneration of the facial nerve. Our objective was to establish normative parameters for both spontaneous and induced whisking and blinking behavior in a large group of normal rats. STUDY DESIGN: Prospective animal study. METHODS: Eighty animals underwent quantitative facial movement testing to measure simultaneous vibrissal movement and ocular closure for each side independently. Right and left C-1 whisker positions were continuously recorded for 5-minute sessions, and changes in infrared detection corresponding to eye closure were continuously recorded. Whisking and blinking were elicited by delivery of olfactory stimuli (10 s scented airflows) and corneal air puffs. Whisks were counted and analyzed, and eye closures were counted. RESULTS: Whisking amplitude, velocity, and acceleration were consistent with literature values. Air puff delivery elicited an ipsilateral blink 99% of the time, a contralateral blink 18% of the time, and changes in or initiation of bilateral whisking 70% of the time. Olfactory stimulus delivery prompted a change in whisking behavior 83% of the time, and eye closure 20% of the time. CONCLUSIONS: This study establishes normative data for assessing cranial nerve VII-controlled facial movement in four separate facial regions. We demonstrate the capability and tendency of animals to move their orbicularis oculi muscles independently of and simultaneously with their midfacial muscles. This model provides an excellent tool for the study of aberrant regeneration after facial nerve injury in the rodent.

A system for studying facial nerve function in rats through simultaneous bilateral monitoring of eyelid and whisker movements.

The occurrence of inappropriate co-contraction (synkinesis) of facially innervated muscles in humans is a common sequela of facial nerve injury and recovery. We have developed a system for studying facial nerve function and synkinesis in restrained rats using non-contact opto-electronic techniques that enable simultaneous bilateral monitoring of eyelid and whisker movements. Whisking is monitored in high spatio-temporal resolution using laser micrometers, and eyelid movements are detected using infrared diode and phototransistor pairs that respond to the increased reflection when the eyelids cover the cornea. To validate the system, 8 rats were tested with multiple 5-min sessions that included corneal air puffs to elicit blink and scented air flows to elicit robust whisking. Four rats then received unilateral facial nerve section and were tested at weeks 3-6. Whisking and eye blink behavior occurred both spontaneously and under stimulus control, with no detectable difference from published whisking data. Proximal facial nerve section caused an immediate ipsilateral loss of whisking and eye blink response, but some ocular closures emerged due to retractor bulbi muscle function. The independence observed between whisker and eyelid control indicates that this system may provide a powerful tool for identifying abnormal co-activation of facial zones resulting from aberrant axonal regeneration.

Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity.

The biomechanics of a motor plant constrain the behavioral strategies that an animal has available to extract information from its environment. We used the rat vibrissa system as a model for active sensing and determined the pattern of muscle activity that drives rhythmic exploratory whisking. Our approach made use of electromyography to measure the activation of all relevant muscles in both head-fixed and unrestrained rats and two-dimensional imaging to monitor the position of the vibrissae in head-fixed rats. Our essential finding is that the periodic motion of the vibrissae and mystacial pad during whisking results from three phases of muscle activity. First, the vibrissae are thrust forward as the rostral extrinsic muscle, musculus (m.) nasalis, contracts to pull the pad and initiate protraction. Second, late in protraction, the intrinsic muscles pivot the vibrissae farther forward. Third, retraction involves the cessation of m. nasalis and intrinsic muscle activity and the contraction of the caudal extrinsic muscles m. nasolabialis and m. maxillolabialis to pull the pad and the vibrissae backward. We developed a biomechanical model of the whisking motor plant that incorporates the measured muscular mechanics along with movement vectors observed from direct muscle stimulation in anesthetized rats. The results of simulations of the model quantify how the combination of extrinsic and intrinsic muscle activity leads to an enhanced range of vibrissa motion than would be available from the intrinsic muscles alone.

Anticipatory activity of motor cortex in relation to rhythmic whisking.

Rats characteristically generate stereotyped exploratory (5-12 Hz) whisker movements, which can also be adaptively modulated. Here we tested the hypothesis that the vibrissal representation in motor cortex (vMCx) initiates and modulates whisking by acting on a subcortical whisking central pattern generator (CPG). We recorded local field potentials (LFPs) in vMCx of behaving Sprague-Dawley rats while monitoring whisking behavior through mystacial electromyograms (EMGs). Recordings were made during free exploration, under body restraint, or in a head-fixed animal. LFP activity increased significantly prior to the onset of a whisking epoch and ended prior to the epoch's termination. In addition, shifts in whisking kinematics within a whisk epoch were often reflected in changes in LFP activity. These data support the hypothesis that vMCx may initiate and modulate whisking behavior through its action on a subcortical CPG.

Whisker motor cortex ablation and whisker movement patterns.

Previous studies, based on qualitative observations, reported that lesions of the whisker motor cortex produce no deficits in whisking behavior. We used high-resolution optoelectronic recording methods to compare the temporal organization and kinematics of whisker movements before and after unilateral lesions of whisker motor cortex in rats. We now report that while the lesion did not abolish whisking, it significantly disrupted whisking kinematics, coordination, and temporal organization. Lesioned animals showed significant increases in the velocity and amplitude of whisker protractions contralateral to the lesions, as well as a reduction in the synchrony of whisker movements on the two sides of the face. There was a marked shift in the distribution of whisking frequencies, with reduction of activity in the 5-7 Hz bandwidth and increased activity at < 2 Hz. Disruptions of the normal whisking pattern were evident on both sides of the face, and the magnitude of these effects was proportional to the extent of the cortical ablation. We suggest that the observed deficits reflect an imbalance in cortical inputs to a brainstem central pattern generator.

Topography of rodent whisking--I. Two-dimensional monitoring of whisker movements.

During 'active touch' the rodent whiskers scan the environment in a series of repetitive movements ('whisks') generating afferent signals which transform the spatial properties of objects into spatio-temporal patterns of neural activity. Based upon analyses carried out in a single movement plane, it has been generally assumed that these trajectories are essentially uni-dimensional, although more complex movements have been described in some rodents. The present study was designed to examine this assumption and to more precisely characterize whisking topography by monitoring whisking trajectories along both the antero-posterior and dorso-ventral axes. Using optoelectronic monitoring techniques with high-spatio-temporal resolution, movement data were obtained from a population of vibrissae sampled at different locations on the mystacial pad in head-fixed rats isolated from the perturbing effects of contact. For a substantial proportion of the population of whisking movements sampled, the trajectories generated by a single whisker is most accurately described as occupying an expended two-dimensional space in which the A-P component predominates. However, the whisker system exhibits a considerable range of trajectory types, suggesting a high degree of movement flexibility. For each vibrissa position, it was possible to delineate a 'trajectory' domain-that portion of the animal's whisking space which is scanned by the movements of that vibrissa during whisking. Since the 'domains' of adjacent whiskers in the same row tend to overlap, synchronized movements of a subset of whiskers could generate a set of overlapping somatosensory fields analogous to overlapping retinal receptive fields. The organization of such trajectory domains within the rats' whisking space could provide the spatial component of the spatio-temporal integration process required to extract information about environmental features from the inputs generated by its recursive whisking movements.

Reversible blockade of rodent whisking: Botulinum toxin as a tool for developmental studies.

Studies of sensorimotor systems such as the whisking system of rodents have suggested that associations between body movements and their sensory consequences during development may make an important contribution to the functional organization of the system. In the present study we have explored the possible utility of Botulinum toxin for developmental studies of whisking. Botox selectively blocks whisking-generated afference leaving other sources of whisker afference intact. We describe appropriate modes of injection, define dosage levels, and assess the effects of prolonged whisking paralysis during development upon the basic motor competency of the adult rat. Our findings indicate that: (a) Botulinum toxin may be used to block whisking behavior in adult and developing rats, (b) that the duration of the whisking paralysis produced by Botox treatment blockade is dose dependent in both developing and adult animals, (c) that the blockade is functionally reversible and (d) that Botox treatment during development does not impair either the kinematics or the rhythmic patterning of adult whisking behavior. Botox may be a useful tool for studying the role of experiential factors in the development of "active touch" in rodents.