Active sensation: insights from the rodent vibrissa sensorimotor system
Introduction
Active touch is a common behavior that animals use to discern the shape, size and texture of objects. The resulting haptic sensations are used to finely tune the position or the motion of tactile sensors. The transformation of sensory inputs into modulatory motor outputs during active touch is performed by sensorimotor feedback loops [1]. Here, we discuss active touch in the context of rhythmic, 5 to 25 Hz whisking by the rat [2] (Figure 1). These animals palpate objects with their vibrissae during a bout (see glossary) of whisking, which lasts for one second or more, to extract a stable picture of the world.
Hutson and Masterton [3] devised sensory tests to isolate perceptual functions of the vibrissae. They found that blind rats with intact vibrissae would leap across wide gaps after contacting the opposite platform with their vibrissae. Rats with clipped vibrissae did not cross these wide gaps. Thus, sensory input from vibrissae enables animals to determine the existence and location of the far side of a gap, in a process that is well suited for electrophysiological studies [4, 5]. A complementary role for the involvement of the vibrissae in detection tasks follows from studies on the discrimination of different textures, in which it is conjectured that rats discriminate with an acuity that rivals that of the human fingertip [6].
Texture is not the only fine sense transduced by the vibrissae. Recent experiments suggest that the vibrissae convey sufficient spatial information to enable rats to distinguish between differently shaped objects [7, 8] and between alleys that differ in width by less than five percent [9, 10].
Section snippets
The rat vibrissa sensorimotor system consists of nested feedback loops
The vibrissae are embedded in feedback loops that form a closed topology at the level of brainstem up through loops that close at the level of the neocortex [11] (Figure 2). Our thesis is that these loops mediate active sensing, which involves a confluence of neuronal signals that represent touch with those that represent vibrissa position.
The brainstem sensorimotor loop is the lowest-order circuit in which sensorimotor integration occurs [12, 13]. It contains secondary sensory nuclei as well
Common scaling for the cortical spike-rate
Here, we have grouped discrimination tasks into two classes. The first class concerns searching for and palpating edges and objects, for which animals exhibit large-angle exploratory whisking in the range of 5 to 15 Hz and foveal whisking up to 25 Hz [2]. Crucially, neurons throughout the entire sensory stream can follow with spike-by-spike precision at these frequencies [60, 61], so that touch signals can be accurately timed relative to the position of the vibrissae. The second class concerns
Conclusions
An analysis of the available data is consistent with the notion of motor control of the vibrissae by sensorimotor loops at the brainstem through cortical levels. Although neural correlates of vibrissa position and touch are already present in the brainstem loop, it appears that the convergence of these signals for object discrimination first occurs within sensory cortex, where we posit that representations of vibrissa position fuse with those of object contact. The available data further imply
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
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Acknowledgements
We thank the Human Frontiers Scientific Program (ME Diamond, D Kleinfeld and E Ahissar), the US-Israeli Binational Science Foundation (E Ahissar and D Kleinfeld), the Center for Theoretical Biological Physics with funding from the National Science Foundation (D Kleinfeld), the Benign Essential Blepharospasm Foundation (D Kleinfeld), the European Community Information Society Technologies Framework Program (ME Diamond), the Telethon Foundation (ME Diamond), the Ministero per l’Istruzione,
Glossary
- Artificial whisking:
- A technique to drive vibrissa motion in the anesthetized animal through electrical stimulation of the relevant branch(es) of the facial nerve.
- Barrels
- Dense clusters of cell bodies, largely stellate neurons, in layer 4 of vibrissa primary sensory cortex. The clusters are arranged in a one-to-one map of the vibrissae and each cluster receives a dense projection from topographically matched cell cluster in ventral posterial medial (VPM-dm) thalamus.
- Bout
- The succession of whisks
References (118)
- et al.
Functional architecture of the mystacial vibrissae
Behav Brain Res
(1997) - et al.
Facial nerve injury induces facilitation of responses in both trigeminal and facial nuclei of rat
Neurosci Lett
(2004) - et al.
Vibrissa deaffentation and rodent whisking patterns: behavioral evidence for a central pattern generator
J Neurosci
(2001) - et al.
Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators
Proc Natl Acad Sci USA
(1997) - et al.
Functional circuits mediating sensorimotor integration: quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons
J Comp Neurol
(2005) - et al.
A major direct GABAergic pathway from zona incerta to neocortex
Science
(1990) - et al.
Intracortical pathways mediate nonlinear fast oscillation (>200 Hz) interactions within rat barrel cortex
J Neurophysiol
(2005) Absence of rapid sensory adaptation in neocortex during information processing states
Neuron
(2004)- et al.
Somatic sensory transmission to the cortex during movement: gating of single cell responses to touch
Exp Neurol
(1982) - et al.
The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units
Brain Res
(1970)
Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells
Cereb Cortex
Closed loop neuronal computations: focus on vibrissa somatosensation in rat
Cereb Cortex
Rhythmic whisking by rat: Retraction as well as protraction of the vibrissae is under active muscular control
J Neurophysiol
The sensory contribution of a single vibrissa's cortical barrel
J Neurophysiol
Enhancement of cortical plasticity by behavioral training in acetylcholine-depleted adult rats
J Neurophysiol
Distribution of tactile learning and its neutral basis
Proc Natl Acad Sci USA
Task-and subject-related differences in sensorimotor behavior during active touch
Somatosens Mot Res
Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks
Somatosens Mot Res
Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations
J Neurosci
Integration of bilateral whisker stimuli in rats: role of the whisker barrel cortices
Cereb Cortex
Anatomical loops and their electrical dynamics in relation to whisking by rat
Somatosens Mot Res
Efferent connections of the brainstem trigeminal complex with the facial nucleus of the rat
J Comp Neurol
The representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat
J Comp Neurol
Topography of whisking II: interaction of whisker and pad
Somatosens Mot Res
Relation between activities of the cortex and vibrissae muscles during high-voltage rhythmic spike discharges in rats
J Neurophysiol
Positive feedback in a brainstem tactile sensorimotor loop
Neuron
Serotonin regulates rhythmic whisking
Neuron
Analysis of sniffing of the albino rat
Behaviour
Facial morphology and vibrissal movement in the golden hamster
J Morphol
The innervation of the mystacial region of the white mouse. A topographical study
J Anat
Changes in motor behavior following the administration of serotonin neurotoxins
Ann N Y Acad Sci
Thalamocortical specificity and the synthesis of sensory cortical receptive fields
J Neurophysiol
Cerebral Cortex: Volume 11: The Barrel Cortex of Rodents
Parallel streams for the relay of vibrissal information through thalamic barreloids
J Neurosci
Distribution of the efferent projections of the rat posterior thalamic nucleus as revealed by phaseolus vulgaris immunohistochemistry
J Hirnforsch
Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus
J Comp Neurol
Transformation from temporal to rate coding in a somatosensory thalamocortical pathway
Nature
Parallel thalamic pathways for whisking and touch signals in the rat
PLoS Biol
New intrathalamic pathways allowing modality-related and cross-modality switching in the dorsal thalamus
J Neurosci
A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus
Nat Neurosci
Coding of stimulus frequency by latency in thalamic networks through the interplay of GABAB-mediated feedback and stimulus shape
J Neurophysiol
Somatosensory corticothalamic projections: distinguishing drivers from modulators
J Neurophysiol
Functional topography of corticothalamic feedback enhances thalamic spatial response tuning in the somatosensory whisker/barrel system
Neuron
The organization of cortico-thalamic pathways: reciprocity versus parity
Brain Res Brain Res Rev
Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row
J Comp Neurol
Single-cell study of motor cortex projections to the barrel field in rats
J Comp Neurol
Adaptive filtering of vibrissa input in motor cortex of rat
Neuron
Evidence for a large projection from the zona incerta to the dorsal thalamus
J Comp Neurol
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