H. Philip Zeigler

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 animals 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.

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 5–7u2009Hz bandwidth and increased activity at <u20092u2009Hz. 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.

Development of rodent whisking: Trigeminal input and central pattern generation

To examine the contribution of whisker inputs to the initial emergence and subsequent refinement of the rodent whisking pattern we combined surgical treatments producing varying degrees of postnatal whisker deafferentation with observations and video analysis of whisking across the first month of life. Whisking emerges during the second postnatal week, preceding eye opening by a few days. In contrast to the absence of deafferentation effects in adults, whisker deafferentation in pups, if carried out between the second and third postnatal week, delays (but does not prevent) the emergence of whisker movements and disrupts the development of normal whisking kinematics and coordination. The extent of the delay varies directly with the reduction in whisker input. When regeneration of the nerve is prevented by a cyanoacrylate block emergence of the normal pattern may be delayed indefinitely. Moreover, section of the whisker motor nerve contralateral to the deafferented side, substantially potentiates the effects of the initial deafferentation. These results confirm and extend an earlier description of the development of whisking in normal rat pups (Welker, Behaviour 12:223–244, ), fix the time of its initial emergence more precisely at P (postnatal day) 11–13, and suggest a critical role for trigeminal afference in the development of the normal whisking pattern. They are discussed in relation to the development of pattern generating mechanisms in the rodent whisker system.

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.

Visual field organization and peck localization in the pigeon (Columba livia)

Some aspects of the stimulus control of peck localization in the pigeon were examined using conditioning paradigms, visual occlusion procedures, and touch-screen technology. Birds were reinforced for pecks made to a small circular (target) stimulus projected upon a computer monitor and located within an electronically defined contingency area. The terminal location of each peck was monitored under binocular and monocular viewing conditions and when using either the frontal or lateral visual fields. Peck localization was highly accurate under either binocular or monocular viewing conditions or with the frontal field alone; there were no systematic differences between the right and left eyes and differences between monocular and binocular localization performance, though significant, were minimal. When viewing with the lateral field alone, subjects were initially unable to locate the food hopper and, even after retraining, conditioned peck localization was profoundly disrupted. The results confirm previous reports of functional differences between the frontal and lateral visual fields, but suggest that monocular cues are sufficient for highly accurate peck localization.

Development of rodent macrovibrissae: Effects of neonatal whisker denervation and bilateral neonatal enucleation

In this paper we describe the effects of manipulating two kinds of sensory input in neonatal rats upon the development of the macrovibrissae—that movable subset of the rodent mystacial vibrissae. In an initial study of normal whisker development, data on whisker size were obtained from neonatal, perinatal, and adult rats. Data on whisker size were also obtained from rats sustaining either neonatal sensory or motor denervation of the whiskers and from both rats and mice bilaterally enucleated as neonates (BEN). In normally reared rats, most whiskers attain their final size over the first three postnatal weeks but development of rows 6 and 7 are not completed until after the first month. In normal animals we found a significant correlation both between body weight and whisker size and between the size of a whisker and the size of its corresponding cortical barrel. Rats sustaining neonatal denervation of the whiskers have shorter and thinner whiskers as adults than normally reared animals. In both rats and mice bilaterally enucleated as neonates a subset of the macrovibrissae are significantly larger than those of normal controls but no such effect is seen if the enucleation is carried out in adults. Moreover, BEN rats exposed to a novel stimulus environment whisk at a significantly higher frequency than normally reared animals. Mechanisms which might mediate these effects are discussed.

Classical conditioning of jaw movements in the pigeon: Acquisition and response topography

Previous studies have shown (1) that the form of the pigeon’s conditioned keypecking response resembles that of its ingestive pecking response, (2) that both ingestive and conditioned pecking in the pigeon are compound responses, including both transport (neck-movement) and gape (jaw-movement) components, and (3) that during operant conditioning or autoshaping of pecking behavior, the gape component comes under the associative control of the CS. In the present study, the gape component was experimentally isolated and a classical conditioning paradigm (water US) was used to bring jaw movements under the control of a CS (light). The results indicate that the topography of the jaw-movement CR is very similar to, though more variable than, that of the UR. They are consistent with the hypothesis that reported similarities in the form of ingestive and conditioned pecking responses reflect, in part, classical conditioning of the gape component.

Conditioned `prehension' in the pigeon: kinematics, coordination and stimulus control of the pecking response

Like human prehensile behavior, the pigeons ingestive pecking response is elicited by visual stimuli conveying information about the location and size of the target. This information is used to generate localized ingestive pecks whose gapes are amplitude-scaled to seed size, prior to contact. We employed high-resolution, real-time monitoring of head acceleration, jaw movements and terminal peck location to examine the kinematics, coordination and stimulus control of conditioned pecking. Conditioning procedures were used to bring pecking under the control of visual targets whose stimulus properties (size, location) were independently varied, while simultaneously monitoring pecking response parameters. Stimulus control of the transport component (peck localization) is extremely precise, even in the absence of a specific localization-dependent reinforcement contingency. Subjects also showed amplitude-scaling of gape size to the size of a visual target, but over a more restricted range than shown to food pellets of comparable sizes. Comparison of the kinematic profiles of conditioned and ingestive pecks suggests that conditioned pecking is functionally analogous to human pointing rather than grasping behavior.

Intracranial self stimulation from endbrain nuclei in the pigeon (Columba livia)

Abstract Intracranial self stimulation (ICSS) may be reliably elicited from several sites in the avian telencephalon, including nucleus basalis, fronto-archistriate tract and palaeostriatal complex. Although key pecking reinforced by brain stimulation has a topography similar to that seen with food reinforcement, food deprivation does not facilitate ICSS at any of the sites. By contrast with olfactory deafferentation which has no effect, trigeminal deafferentation significantly disrupts ICSS. The results are compared with those of previous studies of ICSS in birds and are discussed in relation to the functional organization of the avian telencephalon.

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.