Daniel J. Simons

Responses of Rat Trigeminal Ganglion Neurons to Movements of Vibrissae in Different Directions

The response properties of 123 trigeminal ganglion neurons were studied, using controlled whisker deflections in different directions. When the distal end of the whisker was initially displaced 5.7 degrees (1 mm) from its neutral position, 81% of the cells responded with statistically more spikes/stimulus to movements in one to three of eight cardinal (45 degrees increment) directions than to the others. The more directionally selective the cell, the more vigorous was its response. On the basis of statistical criteria, 75% of the cells were classified as slowly adapting, 25% as rapidly adapting. A number of quantitative analyses indicated that slowly adapting units respond more selectively than rapidly adapting cells to the direction of whisker movement. Differences in directional sensitivities of rapidly and slowly adapting cells appear to parallel differences between their putative mechanoreceptive endings and the relationships between those endings and the vibrissa follicles structure. Comparisons between the response properties of peripheral and central neurons in the vibrissa-lemniscal system indicate that the afferent neural signal is progressively and substantially transformed by mechanisms that function to integrate information from different peripheral receptors and from different, individual vibrissae.

Task- and subject-related differences in sensorimotor behavior during active touch.

Rats explore objects by rhythmically whisking them with their mystacial vibrissae. On two types of tactile discrimination tasks, macrogeometric and microgeometric, better performers palpated the discrimnanda for longer periods of time and used movement patterns that appeared to optimize whisking frequency bandwidth and the extent to which the vibrissae would be bent by object contact. On a task involving finely textured surfaces, good and poor performers differed in the temporal components of their whisking patterns, whereas the spatial domain was more important for animals palpating surfaces with widely separated features. These findings are consistent with increasing neurophysiological evidence that the central representation of the tactile periphery, in rodents and other mammals, is both integrative and dynamic.

Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex.

Recent experimental and theoretical results in cat primary visual cortex and in the whisker-barrel fields of rodent primary somatosensory cortex suggest common organizing principles for layer 4, the primary recipient of sensory input from the thalamus. Response tuning of layer 4 cells is largely determined by a local interplay of feed-forward excitation (directly from the thalamus) and inhibition (from layer 4 inhibitory interneurons driven by the thalamus). Feed-forward inhibition dominates excitation, inherits its tuning from the thalamic input, and sharpens the tuning of excitatory cells. Recurrent excitation enhances responses to effective stimuli.

Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing

Within the rat whisker-to-barrel pathway, local circuits in cortical layer IV are more sensitive to the initial timing of deflection-evoked thalamic responses than to the total number of spikes comprising them. Because thalamic response timing better reflects whisker deflection velocity than amplitude, cortical neurons are more responsive to the former than the latter. The aim of this study is to determine how deflection velocity and amplitude may be encoded by the primary afferent neurons innervating the vibrissae. Responses of 81 extracellularly recorded trigeminal ganglion neurons (60 slowly and 21 rapidly adapting) were studied using controlled whisker stimuli identical to those used previously to investigate the velocity and amplitude sensitivities of thalamic and cortical neurons. For either slowly (SA) or rapidly adapting (RA) neurons, velocity is reflected by both response magnitude, measured as the total number of evoked spikes/stimulus, and initial firing rate, measured as the number of spikes discharged during the first 2 ms of the response. Deflection amplitude, on the other hand, is represented only by the SA population in their response magnitudes. Thus, in both populations initial firing rates unambiguously reflect deflection velocity. Together with previous findings, results demonstrate that information about deflection velocity is preserved throughout the whisker-to-barrel pathway by central circuits sensitive to initial response timing.Within the rat whisker-to-barrel pathway, local circuits in cortical layer IV are more sensitive to the initial timing of deflection-evoked thalamic responses than to the total number of spikes comprising them. Because thalamic response timing better reflects whisker deflection velocity than amplitude, cortical neurons are more responsive to the former than the latter. The aim of this study is to determine how deflection velocity and amplitude may be encoded by the primary afferent neurons innervating the vibrissae. Responses of 81 extracellularly recorded trigeminal ganglion neurons (60 slowly and 21 rapidly adapting) were studied using controlled whisker stimuli identical to those used previously to investigate the velocity and amplitude sensitivities of thalamic and cortical neurons. For either slowly (SA) or rapidly adapting (RA) neurons, velocity is reflected by both response magnitude, measured as the total number of evoked spikes/stimulus, and initial firing rate, measured as the number of spikes discharged during the first 2 ms of the response. Deflection amplitude, on the other hand, is represented only by the SA population in their response magnitudes. Thus, in both populations initial firing rates unambiguously reflect deflection velocity. Together with previous findings, results demonstrate that information about deflection velocity is preserved throughout the whisker-to-barrel pathway by central circuits sensitive to initial response timing.

Functional topography of corticothalamic feedback enhances thalamic spatial response tuning in the somatosensory whisker/barrel system.

Corticothalamic (CT) projections are approximately 10 times more numerous than thalamocortical projections, yet their function in sensory processing is poorly understood. In particular, the functional significance of the topographic precision of CT feedback is unknown. We addressed these issues in the rodent somatosensory whisker/barrel system by deflecting individual whiskers and pharmacologically enhancing activity in layer VI of single whisker-related cortical columns. Enhancement of corticothalamic activity in a cortical column facilitated whisker-evoked responses in topographically aligned thalamic barreloid neurons, while activation of an adjacent column weakly suppressed activity at the same thalamic site. Both effects were more pronounced when stimulating the preferred, or principal, whisker than for adjacent whiskers. Thus, facilitation by homologous CT feedback sharpens thalamic receptive field focus, while suppression by nonhomologous feedback diminishes it. Our findings demonstrate that somatosensory cortex can selectively regulate thalamic spatial response tuning by engaging topographically specific excitatory and inhibitory mechanisms in the thalamus.

A quantitative population model of whisker barrels: Re-examining the Wilson-Cowan equations

Beginning from a biologically based integrate and fire model of a rat whisker barrel, we employ semirigorous techniques to reduce the system to a simple set of equations, similar to the Wilson-Cowan equations, while retaining the ability for both qualitative and quantitative comparisons with the biological system. This is made possible through the clarification of three distinct measures of population activity: voltage, firing rate, and a new term called synaptic drive. The model is activated by prerecorded neural activity obtained from thalamic “barreloid” neurons in response to whisker stimuli. Output is produced in the form of population PSTHs, one each corresponding to activity of spiny (excitatory) and smooth (inhibitory) barrel neurons, which is quantitatively comparable to PSTHs from electrophysiologically studied regular-spike and fast-spike neurons. Through further analysis, the model yields novel physiological predictions not readily apparent from the full model or from experimental studies.

Neuronal Integration in the Somatosensory Whisker/Barrel Cortex

Seminal studies of the physiological organization of the somatosensory cortex of cats and monkeys suggested that it was comprised of replicated, local neuronal circuits which process afferent information from the thalamus (Mountcastle, 1957; Mountcastle and Powell, 1959). Subsequently, investigations of different cortical areas in a variety of species supported these conclusions by confirming that neurons that are located in vertical register with each other typically have similar receptive field properties and that certain of these properties change, sometimes rather abruptly, with horizontal position in the cortical tissue. The visualization of strikingly regular anatomic patterns in some cortical areas has reinforced the concept of iterated modularity as a fundamental principle of cortical organization. Though the defining characteristics of modules in different cortical regions are not consistent (Purves et al., 1992), a recent comprehensive review by White and Keller (see White, 1989) has identified rules of synaptic connectivity which form the basis of local cortical circuits, and these are likely to be applicable regardless of the gross morphological features of a particular cortical region. Increasingly there is a recognition that, even in primary sensory areas, local circuits are capable of changing in response to short- as well as long-term demands of the sensory environment. Indeed, several influential theories of cortical function ascribe a critical role to dynamic behaviors of neuronal assemblies, whether they be of a local or a distributed nature (Hebb, 1949; Mountcastle, 1979; Edelman, 1987).

Membrane potential changes in rat SmI cortical neurons evoked by controlled stimulation of mystacial vibrissae

Intracellular recordings from rat somatic sensory vibrissa/barrel cortex demonstrate that whisker displacements evoke short latency excitatory postsynaptic potentials followed by longer lasting inhibitory potentials. The time course and whisker-related spatial distribution of the potentials represent synaptic correlates of the integration of whisker inputs observed in extracellular studies.

Motor modulation of afferent somatosensory circuits

A prominent feature of thalamocortical circuitry in sensory systems is the extensive and highly organized feedback projection from the cortex to the thalamic neurons that provide stimulus-specific input to the cortex. In lightly sedated rats, we found that focal enhancement of motor cortex activity facilitated sensory-evoked responses of topographically aligned neurons in primary somatosensory cortex, including antidromically identified corticothalamic cells; similar effects were observed in ventral posterior medial thalamus (VPm). In behaving rats, thalamic responses were normally smaller during whisking but larger when signal transmission in brainstem trigeminal nuclei was bypassed or altered. During voluntary movement, sensory activity may be globally suppressed in the brainstem, whereas signaling by cortically facilitated VPm neurons is simultaneously enhanced relative to other VPm neurons receiving no such facilitation.

Functional organization of mouse and rat SmI barrel cortex following vibrissal damage on different postnatal days.

This study was undertaken to determine the functional properties of neurons in the anatomically altered somatosensory cortex after neonatal whisker damage. In mice and rats neonatal lesions of the facial vibrissae change the anatomical organization of barrels in the contralateral SmI cortex. These changes depend on the pattern and severity of the peripheral damage and the developmental age of the animals. To understand some of the functional correlates of these anatomical changes, the middle row of vibrissae (row C) was damaged in mice on postnatal days 1, 3, and 5 and in rats on postnatal days 1 and 5. The receptive field properties of single cortical units were studied after the animals matured. In 24 mice and 15 rats a total of 1,370 units were characterized in microelectrode penetrations which passed through the somatosensory cortex either tangential or perpendicular to the pia. Units were localized anatomically with respect to both barrel and laminar boundaries, and the extent of the peripheral damage was assessed histologically. The data revealed an orderly representation of the sensory periphery that coincided with the altered cytoarchitectonic organization of the SmI cortex. Specifically: (1) Units in the enlarged row B or row D barrels responded primarily to row B or row D whiskers. (2) In layer IV, units in the altered row C cortex either could not be reliably driven from the periphery, were activated by stimulation of scar tissue in the damaged facial row C, or were driven by adjacent, intact row B or row D whiskers. (3) Units in supra- and infragranular layers either had no row C representation or incorporated scar tissue in their receptive fields in a topographically correct fashion. Responses of units to stimulation of scar tissue were qualitatively similar to those elicited from intact vibrissae, which also activated them. (4) In SmII, units that responded to whiskers had receptive fields whose organization matched the representation of the periphery observed in SmI. (5) There was no mapping of nonmystacial pad structures in the barrel cortex, and there were no units with abnormal multiwhisker interactions when laminar boundaries were taken into account. These data indicate that neonatal damage to the whiskers alters both the anatomical arrangement of the barrels and the physiologically determined somatotopic representation of the sensory periphery in a parallel and predictable fashion.