Coding of apparent motion in the thalamic nucleus of the rat vibrissal somatosensory system.

While exploring objects, rats make multiple contacts using their whiskers, thereby generating complex patterns of sensory information. The cerebral structures that process this information in the somatosensory system show discrete patterns of anatomically distinct units, each corresponding to one whisker. Moreover, the feedforward and feedback connections are remarkably topographic, with little cross-whisker divergence before reaching the cortical network. Despite this parallel design, information processing from several whiskers has been reported in subcortical nuclei. Here, we explored whether sensory neurons in the ventral posterior medial nucleus (VPM) of the thalamus encode emergent properties of complex multiwhisker stimulations. Using a 24-whisker stimulator, we tested the responses of VPM neurons to sequences of caudal deflections that generated an apparent motion in eight different directions across the whiskerpad. Overall, 45% of neurons exhibited an evoked increase in firing rate significantly selective to the direction of apparent motion of the global stimulus. Periods of suppression of firing rate were often observed, but were generally not selective. Global motion selectivity of VPM neurons could occur regardless of the extent and spatial organization of their receptive fields, and of their selectivity for the direction of motion of their principal whisker. To investigate whether the global selectivity could be due to corticothalamic feedback connections, we inactivated the barrel cortex while repeating the stimulation protocol. For most VPM neurons, the direction selectivity decreased but was still present. These results suggest that nonlinear processing of stimuli from different whiskers emerges in subcortical nuclei and is amplified by the corticofugal feedback.

Spatial structure of multiwhisker receptive fields in the barrel cortex is stimulus dependent.

The tactile sensations mediated by the whisker-trigeminal system allow rodents to efficiently detect and discriminate objects. These capabilities rely strongly on the temporal and spatial structure of whisker deflections. Subthreshold but also spiking receptive fields in the barrel cortex encompass a large number of vibrissae, and it seems likely that the functional properties of these multiwhisker receptive fields reflect the multiple-whisker interactions encountered by the animal during exploration of its environment. The aim of this study was to examine the dependence of the spatial structure of cortical receptive fields on stimulus parameters. Using a newly developed 24-whisker stimulation matrix, we applied a forward correlation analysis of spiking activity to randomized whisker deflections (sparse noise) to characterize the receptive fields that result from caudal and rostral directions of whisker deflection. We observed that the functionally determined principal whisker, the whisker eliciting the strongest response with the shortest latency, differed according to the direction of whisker deflection. Thus, for a given neuron, maximal responses to opposite directions of whisker deflections could be spatially separated. This spatial separation resulted in a displacement of the center of mass between the rostral and caudal subfields and was accompanied by differences between response latencies in rostral and caudal directions of whisker deflection. Such direction-dependent receptive field organization was observed in every cortical layer. We conclude that the spatial structure of receptive fields in the barrel cortex is not an intrinsic property of the neuron but depends on the properties of sensory input.

The Matrix: a new tool for probing the whisker-to-barrel system with natural stimuli.

The whisker to barrel system in rodents has become one of the major models for the study of sensory processing. Several tens of whiskers (or vibrissae) are distributed in a regular manner on both sides of the snout. Many tactile discrimination tasks using this system need multiple contacts with more than one whisker to be solved. With the aim of mimicking those multi-whisker stimuli during electrophysiological recordings, we developed a novel mechanical stimulator composed of 24 independent multi-directional piezoelectric benders adapted to the five rows and the five caudal arcs of the rat whisker pad. The most widely used technology for producing mechanical deflections of the whiskers is based on piezoelectric benders that display a non-linear behavior when driven with high frequency input commands and, if not compensated, show high unwanted ringing at particular resonance frequencies. If not corrected, this non-linear behavior precludes the application of high frequency deflections and the study of cortical responses to behaviorally relevant stimuli. To cope with the ringing problem, a mechanical and a software based solutions have been developed. With these corrections, the upper bound of the linear range of the bender is increased to 1 kHz. This new device allows the controlled delivery of large scale natural patterns of whisker deflections characterized by rapid high frequency vibrations of multiple whiskers.

Emergent properties of tactile scenes selectively activate barrel cortex neurons.

Rats discriminate objects by scanning their surface with the facial vibrissae, producing spatiotemporally complex sequences of tactile contacts. The way in which the somatosensory cortex responds to these complex multivibrissal stimuli has not been explored. It is unclear yet whether contextual information from across the entire whisker pad influences cortical responses. Here, we delivered tactile stimuli to the rat vibrissae using a new 24 whisker stimulator. We tested sequences of rostrocaudal whisker deflections that generate multivibrissal motion patterns in different directions across the mystacial pad, allowing to disambiguate local from global sensory integration. Unitary electrophysiological recordings from different layers of the barrel cortex showed that a majority of neurons has direction selectivity for the multivibrissal stimulus. The selectivity resulted from nonlinear integration of responses across the mystacial pad. Our results indicate that the system extracts collective properties of a tactile scene.

Evidence for a direct subthalamo-cortical loop circuit in the rat.

The subthalamic nucleus (STN), a major component of the basal ganglia (BG), plays a crucial role in motor activity and cognitive functions. In current models of the BG, the STN is considered to act by activating the gamma-aminobutyric acid (GABA)ergic neurons of the BG output nuclei, thus inhibiting their thalamic and brain stem targets. However, in addition to the BG output nuclei, the STN has also been reported to innervate the cerebral cortex and the striatum. Here, the anatomo-functional organization of STN projections to the cerebral cortex was investigated using anatomical and electrophysiological approaches. First, wheatgerm agglutinin-conjugated horseradish peroxidase was injected into defined areas of the cerebral cortex to analyse the spatial distribution of retrogradely labelled STN neurons. The mode of cortical innervation by the STN was then determined using extracellular deposits of Phaseolus vulgaris-leucoagglutinin into the STN. Finally, the functional organization of the cortico-STN relationships was investigated by extracellularly recording single STN units antidromically driven from the cerebral cortex. Our results indicate that STN innervates the sensory-motor and prefrontal cortices, the densest projections terminating in cortical layers I-III of the orofacial motor area. The matching between the topographic distribution of subthalamo-cortical neurons and cortico-subthalamic projections forms the basis of a functional cortico-STN loop circuit that is partially opened. In pathological situations such as Parkinson's disease and epilepsy, the STN-cortex loop circuit might contribute to propagate pathological oscillations favouring the emergence of abnormal synchronized activities and a loss of functional selectivity in the cortico-BG network.