Behavioral Properties of the Trigeminal Somatosensory System in Rats Performing Whisker-Dependent Tactile Discriminations (original) (raw)
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The Matrix: A new tool for probing the whisker-to-barrel system with natural stimuli
Journal of Neuroscience Methods, 2010
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 nonlinear 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.
Integration of Multiple-whisker Inputs in Rat Somatosensory Cortex
Cerebral Cortex, 2001
Rats explore their surroundings through rhythmic movement of their mystacial vibrissae. At any given moment, multiple whiskers are simultaneously moved and may contact the surface of an object. The aim of this work is to understand how simultaneous multiple-whisker deflections are processed in the somatosensory cortex. Arrays of 25 electrodes were inserted into the vibrissal representation of barrel cortex of adult rats. Multi-unit responses were recorded during (i) stimulation of single whiskers, and (ii) simultaneous stimulation of two, three or four whiskers of a whisker arc or whisker row. The whole-array response elicited by the simultaneous stimulation of multiple-whiskers (observed response) was compared to a multiple-whisker response predictor, defined as the sum of the whole-array responses to the separate stimulation of the corresponding single whiskers. The observed response to stimulation of four whiskers was nearly always less than the predicted response, indicating a sublinear summation of multiple coincident inputs. Examining the poststimulus time course of sublinearity, we found that the earliest cortical response to whisker deflection -reflecting the thalamocortical volley -was linear, whereas the successive cortical response was highly sublinear. This suggests a cortical origin of the phenomenon.
Somatosensory & Motor Research, 2001
We compared whisking movement patterns during acquisition of tactile detection and object discrimination under conditions in which (a) head movements are excluded and (b) exposure to tactile discriminanda is confined to the large, moveable vibrissae (macrovibrissae). We used optoelectronic instrumentation to track the movements of an individual whisker with high spatio-temporal resolution and a testing paradigm, which allowed us to dissociate performance on an ª indicatorº response (lever pressing) from the rat's ª observingº responses (discriminative whisking). We analyzed the relation between discrimination performance and whisking movement patterns in order to clarify the process by which the indicator response comes under the stimulus control of information acquired by the rat's whisking behavior. Whisking patterns over the course of task acquisition differed with task demands. Acquisition of the Detection task was correlated with modulation of only one whisking movement parameterÐ total number of whisks emitted, and more whisking was seen on trials in which the discriminandum was absent. Discrimination between a sphere and cube differing in size and texture was correlated with a reduction in whisk duration and protraction amplitude and with a shift towards higher whisking frequencies. Our findings confirm previous reports that acquisition of tactile discriminations involves modulation by the animal of both the amount and the type of whisking. In contrast with a previous report (Brecht et al., 1997), they indicate that rats can solve tactile object detection and discrimination tasks (a) using only the large, motile mystacial vibrissae (macrovibrissae) and (b) without engaging in head movements. We conclude that the functional contribution of the macrovibrissae will vary with the nature of the task and the conditions of testing.
Texture discrimination and unit recordings in the rat whisker/barrel system
Physiology & Behavior, 2002
We have developed a semi-automated technique for acquiring neurophysiological data during whisker-based tactile discriminative behavior. Water-deprived, blindfolded rats are tethered by means of a harness vest that permits them to contact a rough (250 μm grooves) or smooth discriminandum with only their vibrissae. Discriminanda are mounted on a motor-driven carousel, and the rat indicates its choice (rough, smooth) by licking either a right or left water port located near the carousel. A narrow light beam detects general proximity of the animal's nose to the discriminandum, although actual whisker contact is monitored by a SuperVHS camera and measured offline using field-by-field videographic analysis. Rats can be trained within 3–6 weeks at which time they perform 100–150 trials/day at a level of 80% correct. Unit recording from the somatosensory cortex reveals that neurons increase their firing upon whisker contact of a discriminandum and that firing remains elevated during several hundred milliseconds of ongoing contact, even with the smooth surface. Nevertheless, despite the animal's ability to distinguish the rough and smooth surfaces, overall neuronal firing rates were indistinguishable for the two surfaces. In some cases, temporal firing patterns differed, although not in a consistent way across recording sites.
Journal of Neurophysiology, 2005
Rats explore their environment by actively moving their whiskers. Recently, we described how object location in the horizontal (front-back) axis is encoded by first-order neurons in the trigeminal ganglion (TG) by spike timing. Here we show how TG neurons encode object location along the radial coordinate, i.e., from the snout outward. Using extracellular recordings from urethane-anesthetized rats and electrically induced whisking, we found that TG neurons encode radial distance primarily by the number of spikes fired. When an object was positioned closer to the whisker root, all touch-selective neurons recorded fired more spikes. Some of these cells responded exclusively to objects located near the base of whiskers, signaling proximal touch by an identity (labeled-line) code. A number of tonic touch-selective neurons also decreased delays from touch to the first spike and decreased interspike intervals for closer object positions. Information theory analysis revealed that near-certainty discrimination between two objects separated by 30% of the length of whiskers was possible for some single cells. However, encoding reliability was usually lower as a result of large trial-by-trial response variability. Our current findings, together with the identity coding suggested by anatomy for the vertical dimension and the temporal coding of the horizontal dimension, suggest that object location is encoded by separate neuronal variables along the three spatial dimensions: temporal for the horizontal, spatial for the vertical, and spike rate for the radial dimension.
2004
Copyright © 2004 by the American Physiological Society. 2 Bilateral single-unit recordings in primary somatosensory cortex (S1) of anesthetized rats have revealed substantial cross-talk between cortical hemispheres (Shuler, 2001), suggesting the possibility that behaviorally relevant bilateral integration could occur in S1. To determine the extent of bilateral neural responses in awake animals, we recorded S1 multi- and single-unit activity in head-immobilized rats while stimulating groups of 4 whiskers from the same column on both sides of the head. Results from these experiments confirm the widespread presence of single units responding to tactile stimuli on either side of the face in S1 of awake animals. Quantification of bilateral integration by multiunits revealed both facilitative and suppressive integration of bilateral inputs. Varying the interval between left and right whisker stimuli between 0 and 120 ms showed the temporal integration of bilateral stimuli to be dominated ...
Journal of Neurophysiology, 2005
Bilateral single-unit recordings in primary somatosensory cortex (S1) of anesthetized rats have revealed substantial cross talk between cortical hemispheres, suggesting the possibility that behaviorally relevant bilateral integration could occur in S1. To determine the extent of bilateral neural responses in awake animals, we recorded S1 multi- and single-unit activity in head-immobilized rats while stimulating groups of 4 whiskers from the same column on both sides of the head. Results from these experiments confirm the widespread presence of single units responding to tactile stimuli on either side of the face in S1 of awake animals. Quantification of bilateral integration by multiunits revealed both facilitative and suppressive integration of bilateral inputs. Varying the interval between left and right whisker stimuli between 0 and 120 ms showed the temporal integration of bilateral stimuli to be dominated on average by suppression at intervals around 30 ms, in agreement with co...
Precise Temporal Responses in Whisker Trigeminal Neurons
Journal of Neurophysiology, 2004
The ability of rats using their whiskers to perform fine tactile discrimination rivals that of humans using their fingertips. Rats must perform these discriminations rapidly and accurately while palpating the environment with their whiskers. This suggests that whisker-derived inputs produce a robust and reliable code, capable of capturing complex, high-frequency information. The first neural representation of whisker-derived stimulus information is in primary afferent neurons of the trigeminal ganglion. Here we demonstrate that there is a continuum of directiondependent response profiles in trigeminal neurons and provide the first quantitative analysis of the encoding of complex stimuli by these neurons. We show that all classes of trigeminal ganglion neurons respond with highly reproducible temporal spike patterns to transient stimuli. Such a robust coding mechanism may allow rapid perception of complex tactile features.