John M. Gibson

Fractured Somatotopy in Granule Cell Tactile Areas of Rat Cerebellar Hemispheres Revealed by Micromapping; pp. 94–105

We defined spatial patterns of tactile projections to cerebellar cortex of anesthetized albino rats using microelectrode micromapping methods. Low threshold natural stimulation of cutaneous mechanorec

Principles of organization of a cerebro-cerebellar circuit. Micromapping the projections from cerebral (SI) to cerebellar (granule cell layer) tactile areas of rats.

We defined spatial patterns of organization of projections from somatosensory cerebral cortex (SI) to the somatosensory cerebellar cortex of anesthetized albino rats using microelectrode (stimulation and recording) micromapping methods and low-threshold cutaneous (tactile) stimulation. Two sampling strategies were used: (1) a single cerebral SI locus in layers V-VI was stimulated electrically, while a responding region of the cerebellar granule cell (GC) layer was systematically mapped with a recording electrode; (2) the SI stimulating electrode was used as the mapping electrode while the cerebellar GC electrode remain fixed. We found highly specific patterns of connections between somatotopically organized SI cortex and the somatotopically fractured tactile cerebellar cortex. Using threshold stimulating currents in SI, the projections from small populations of neural elements were found to be highly restricted, terminating within the confines of only those tactile cerebellar hemispheric locations having the same receptive fields (RFs). These SI-GC projections conform to the patchy mosaic pattern of organization previously shown for peripheral tactile projections. SI projections to GC patches were either contralateral or ipsilateral, depending on the laterality of the peripheral projections to that patch. Each SI focus projected to only a portion of a patch; projections from several adjacent SI loci overlapped serially within a patch. As with the peripherally evoked GC layer responses, SI-evoked GC responses were organized in a columnar fashion and were maximal at middle levels of the GC layer; SI-GC latencies were 5-8 ms. These data reveal that this tactile-related cerebro-cerebellar circuit exhibits precisely organized patterns of projection.

Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 1. Receptive field properties and threshold distributions.

We examined stimulus-response relationships of vibrissa-activated mechanosensory neurons of the rats fifth (trigeminal) ganglion. Single-unit activity was recorded with tungsten microelectrodes. The vibrissae were deflected with a variety of parametrically controlled stimulus waveforms. We found that the receptive field of each vibrissa-activated neuron consisted of a single vibrissa. Few, if any, unambiguous examples of spontaneous activity were observed in these neurons. Even if true spontaneous activity was present, its observed incidence was low, as were the measured discharge rates. Thresholds of individual neurons were usually quite discrete; often a 1-2% increase in pulse magnitude (angular displacement) above a level to which the neuron did not respond caused it to discharge on every trial. The distribution of thresholds for the sample was continuous with a median of about 1 degree and a range of over three orders of magnitude. The most sensitive neurons responded to deflections of less than 0.1 degrees. Many neurons responded to a single suprathreshold pulse with more than one spike. We found no consistent relationships among the thresholds of the additional evoked discharges of an individual neuron other than that the total number of evoked spikes either increased or stayed the same, but never decreased, as stimulus magnitude increased. About one-third of the neurons examined had velocity thresholds below 3 degrees/sec. Above that value, thresholds were distributed continuously throughout a range of over three orders of magnitude. The median velocity threshold was about 100 degrees/sec. The broad and continuous distributions of both magnitude and velocity thresholds suggest that a population of vibrissa-activated neurons can code stimulus strength smoothly and continuously over a wide range, even though individual neurons may be poorly suited to do so.

Tactile projections to granule cells in caudal vermis of the rat's cerebellum.

We discovered a small tactile area in a single a folium of the uvula of the cauday vermis of the rats cerebellum. Gentle mechanical stimulation of relatively small cutaneous receptive fields (RFs) activated multiple units in the granule cell (GC) layer in a portion of a single folium in rats anesthetized with sodium pentobarbital. The total size of this area on each side of the midline is about 1.5 mm2, yet micromapping within this tiny region using tungsten ball microelectrodes and a high puncture sampling density (about 75 punctures/mm2) revealed a highly differentiated pattern of cutaneous projections to the GC layer. All peripheral projections are ipsilateral; the two homologous areas from each side adjoining at the midline of folium 9a. The larger projection areas from cutaneous RFs are mostly from mystacial vibrissae and upper lip, but small projection sites from the remainder of the head, neck and forelimb also are present. The pattern of projections were patch-like, forming a fractured somatotopic pattern or mosaic, with some somatotopic and some nonsomatotopic features. Each RF activated units in a vertical column in the GC layer. This area has not been described in any mammal, and its functional role can now be studied.

Corticofugal influences in the rat on responses of neurons in the trigeminal nucleus interpolaris to mechanical stimulation

We recorded effects of electrical stimulation of sensorimotor cortex on the responses of 45 neurons in the interpolar trigeminal nucleus to mechanical stimulation of vibrissae. Responses elicited by peripheral mechanical stimulation were enhanced when a neurons receptive field (RF) included the RF of the cortical stimulating locus, and suppressed when the RFs of the cortical site and the interpolar neuron did not overlap. Several interpolaris neurons influenced by cortical stimulation were shown to project to the cerebellum.

Diversity of coding profiles of mechanoreceptors in glabrous skin of kittens

We examined stimulul-response (S-R) profiles of 35 single mechanoreceptive afferent units having small receptive fields in glabrous forepaw skin of 24 anesthetized domestic kittens. Single unit activity was recorded with tungsten microelectrodes from cervical dorsal root ganglia. The study was designed to be as quantitatively descriptive as possible. We indented each units receptive field with a broad battery of simple, carefully controlled stimuli whose major parameters, including amplitude, velocity, acceleration, duration, and interstimulus interval were systematically varied. Stimuli were delivered by a small probe driven by a feedback-controlled axial displacement generator. Single unit discharge data were analyzed by a variety of direct and derived measures including dot patterns, peristimulus histograms, instantaneous and mean instantaneous firing rates, tuning curves, thresholds for amplitude and velocity, adaptation rates, dynamic and static sensitivities, and others. We found that with respect to any of the S-R transactions examined, the properties of our sample of units were continuously and broadly distributed. Any one unit might exhibit either a slow or rapid rate of adaptation, or might superficially appear to preferentially code a single stimulus parameter such as amplitude or velocity. But when the entire range of responsiveness of units to the entire stimulus battery was surveyed by a variety of analytic techniques, we were unable to find any justifiable basis for designation of discrete categories of S-R profiles. Intermediate response types were always found, and in general, all units were both broadly tuned and capable of responding to integrals of several stimulus parameters, our data argue against the usefulness of evaluating a units S-R coding capabilities by means of a limited ste of stimulation of response analysis procedures.

Functional development of mechanoreceptive neurons innervating the glabrous skin in postnatal kittens

We studied single units innervating the glabrous forepaw skin of 35 domestic kittens ranging in age from 1 to 52 postnatal days. There aspects of coding were emphasized: (a) size and force thresholds of receptive fields, (b) time course of recovery between stimulus presentations, and (c) electrical conduction properties of the afferent nerve fibers. Receptive field (RF) size and force thresholds were (a) positively correlated with age for palmar but not digital RFs, and (b) were significantly larger on palm than on digits. Unit responsiveness was highly dependent on intertrial interval, complete recovery requiring at least 30 sec. Conduction velocity increased more rapidly than nerve fiber length, thus conduction time decreased with age. Refractory period decreased with age, but the conduction velocities of sequential spikes were proportional, regardless of age. These changes which we observed can more readily be ascribed to alterations of the mechanical properties of skin and conduction properties of nerve fibers than to changes in the coding mechanisms themselves.

Stimulus-response profile analysis: a comprehensive, quantitative approach to the study of sensory coding and information processing

In order to understand the coding and information processing capabilities of mechanosensory neurons, it is necessary to examine stimulus--response relationships under a wide variety of stimulus conditions, using a comprehensive set of quantitative analytic procedures. We employ the methodology of stimulus--response profile analysis, which is based on 4 principles: (1) the use of a broad-based battery of quantitatively controlled mechanical stimuli; (2) maintenance of comprehensive records of experiments; (3) detailed, quantitative analysis of single-unit responses; and (4) the application of these principles uniformly and consistently to all units studied. In addition to conventional graphical portrayals of single-unit activity, we employ a set of quantitative response indices, each of which represents a particular aspect of a units overall responsiveness. The distribution of a response index for the entire sample of neurons examined in a particular population offers insight into the manner in which a specific stimulus feature is presented within that population. The distributions of response indices obtained from different neural populations can be compared statistically in order to evaluate interpopulation differences in stimulus-response relationships. This comprehensive, quantitative approach is capable of demonstrating significant, although subtle, interpopulation differences which are not revealed by more cursory, qualitative methods.