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'Where' and 'what' in the whisker sensorimotor system

A Corrigendum to this article was published on 01 September 2008

Key Points

  • The first study of whisker function, from 1912, showed that rats lose the capacity to navigate in a complex labyrinth if their whiskers are clipped. The tactile modality is crucial to the behavioural repertoire of most rodent species.

  • Rats and mice generate their sense of touch through active movement of their whiskers. From signals that originate in sensory receptors at the base of the whisker, the brain builds up representations of the location and identity of contacted objects.

  • The modern era of research into whisker function began in 1970 with the discovery of cortical barrels, which are clusters of densely-packed cells that anchor a columnar module dedicated to one whisker. Barrels are organized as a map that conserves the spatial relationships between whiskers.

  • Since the discovery of cortical barrels, further investigations have unravelled the functional circuitry of the sensory pathways from whiskers to the cortex. Most work has come from anaesthetized animals.

  • Researchers are now trying to learn how animals use their whiskers under natural conditions, and how the surrounding world is represented in their brains. Objects can be considered according to their location ('where') and their identity ('what').

  • As examples of localization tasks, we consider rats' capacities to sense the size of an opening between two walls and the forward–backward position of vertical poles. Sensorimotor strategy — that is, how the animal whisks and how it uses signals from multiple whiskers — differs according to the task.

  • The neuronal representation of object location involves the integration of the response to object contact with a reference signal that reports the position of the whisker at the instant of contact. Reference signals originate from sensory receptors, but the motor system could also provide information about whisker position.

  • As examples of object identification tasks, we consider rats' capacities to sense shape and texture; in both of these, rats are highly proficient. The Etruscan shrew uses its whiskers to identify insect prey by shape.

  • In rats, the texture of a contacted surface is encoded by neuronal firing rate; rougher surfaces evoke higher firing rates. On single trials, firing rate correlates with the animal's judgment of texture.

  • Because the strength of the animal's own motor output will affect the strength of the sensory response, we hypothesize that the animal uses knowledge of motor output to interpret the firing rate on individual contacts. A numerical model illustrates how knowledge of motor output makes sensory judgments more accurate.

  • Three problems are particularly fascinating for future research. How are whisker dynamics reported by neuronal activity in behaving animals? Where in the sensory system are the 'where' and 'what' signals separated? How are neuronal representations transformed from stages at which they encode physical signals to stages at which they encode things that are meaningful to the animal?

Abstract

In the visual system of primates, different neuronal pathways are specialized for processing information about the spatial coordinates of objects and their identity — that is, 'where' and 'what'. By contrast, rats and other nocturnal animals build up a neuronal representation of 'where' and 'what' by seeking out and palpating objects with their whiskers. We present recent evidence about how the brain constructs a representation of the surrounding world through whisker-mediated sense of touch. While considerable knowledge exists about the representation of the physical properties of stimuli — like texture, shape and position — we know little about how the brain represents their meaning. Future research may elucidate this and show how the transformation of one representation to another is achieved.

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Figure 1: Layout of the whisker sensory pathway.
Figure 2: Bilateral comparison of horizontal object localization.
Figure 3: Absolute horizontal object localization.
Figure 4: Object recognition by shape.
Figure 5: Texture discrimination task.
Figure 6: The role of motor signals in decoding sensory inputs.

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Acknowledgements

The authors would like to thank their many brilliant and helpful colleagues, too numerous to list. The joint efforts of the senior authors (M.E.D., D.K. and E.A.) have been supported by Human Frontier Science Program grant RG0043/2004-C. M. E. D. additionally recognizes the support of EC grant BIOTACT (ICT-215910), Ministero per l'Istruzione, l'Università e la Ricerca grant 2006050482_003, Regione Friuli Venezia Giulia and the Italian Institute of Technology.

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Glossary

Surface texture

Texture relates to the surface pattern of objects. Roughness is one of the attributes of texture. The roughness of an irregular sandpaper-like surface texture is quantified by its grain size; the larger the grains, the coarser the texture.

Barrel

A set of neurons in the somatosensory cortex. Each barrel is responsible for processing the input from one whisker.

Macrovibrissae

Long (3–40 mm), sparsely spaced (2 per cm2) whiskers located on the middle and posterior part of a rat's snout. They are ordered in a regular, geometric grid and exhibit prominent forward and backward whisking motion.

Hyperacuity

Sensory acuity that exceeds the spatial resolution of the sensor. Vibrissal hyperacuity is the ability to resolve spatial offsets that are smaller than the inter-vibrissal spacing.

Sensory receptor neuron

Neuron that converts a physical stimulus into electric impulses. In the whisker system, the cells of the trigeminal ganglion act as sensory receptor neurons.

Temporal code

A coding scheme where not only the rate of action potentials is informative, but also their firing pattern. Two stimuli which evoke the same firing rate may be discriminated if they evoke unique firing patterns.

Spatial-coding

A coding scheme where the position of the active neuron carries critical information. For example, if C3 neurons fire, the stimulus location is specified as being in the trajectory of the C3 whisker. This type of coding is sometimes called 'identity coding'.

Rate-coding

A coding scheme where a stimulus' quality, such as its intensity, is transmitted by the quantity of spikes emitted per unit of time.

Microvibrissae

Short (few mm), densely spaced (87 per cm2) whiskers located on the anterior part of a rats snout. They are not ordered in a regular grid and exhibit little or no whisking motion.

Kinetic signature

The temporal profile of a whisker's movement as it slides across a texture. It is characteristic of the texture, modulated by sliding speed and whisker length (among other factors), and appears to be quite robust.

Principal whisker

The whisker that upon stimulation evokes the strongest response in a given sensory neuron.

d′

(d prime). A measure of the discriminability of two stimuli. If the stimuli differ with respect to some quantity, d′ is defined as the difference between the means divided by the standard deviations.

Electromyography

Recording of electrical activity generated by the muscle.

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Diamond, M., von Heimendahl, M., Knutsen, P. et al. 'Where' and 'what' in the whisker sensorimotor system. Nat Rev Neurosci 9, 601–612 (2008). https://doi.org/10.1038/nrn2411

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