Active sensation: insights from the rodent vibrissa sensorimotor system

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Rats sweep their vibrissae through space to locate objects in their immediate environment. In essence, their view of the proximal world is generated through pliable hairs that tap and palpate objects. The texture and shape of those objects must be discerned for the rat to assess the value of the object. Furthermore, the location of those objects must be specified with reference to the position of the rat's head for the rat to plan its movements. Recent in vivo and in vitro electrophysiological measurements provide insight into the algorithms and mechanisms that underlie these behavioral-based computations.

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:

  • • of special interest

  • •• of outstanding interest

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

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