Primer Whisker-Mediated Texture Discrimination

Our sense of touch provides information about nearby objects that can affect us in an immediate way. Texture, a central component of touch, is sensed quickly, even before an object is explored to measure its size, shape, or identity. To learn how contact with a surface produces a sensation of texture, many laboratories have examined the whisker system of rodents. Touch sensed through the whiskers in rodents works differently than touch sensed through the fingertips in primates. Touch receptors in the fingertips are distributed in a continuous sheet; this spatial distribution of inputs gives important signals about texture [1]. In contrast, rodents use a set of roughly 30 whiskers on each side of the snout, palpating surfaces through a 5–15 Hz forward-backward motion known as “whisking.” When a whisker’s tip or shaft makes contact with a texture, its movement changes; whisker motion signals report to the brain what the whiskers have contacted. The performance of rats in discriminating textures is astonishing. In the dark, they can extract the identity of a texture based on just one to three touches per whisker and can display accurate judgments of a texture within 100 ms of initial whisker contact [2]. Whisker-mediated texture discrimination has many lessons to teach neuroscientists about sensor mechanisms, central encoding, and the transformation of sensory representations to behavioral output. It is not surprising, then, that whisker touch has become a focus of engineers who look to biology for inspiration in their attempt to endow robots with sense of touch (see, for example, http://www.biotact.org/). This Primer summarizes our current understanding of how whisker motion becomes, for the animal, a texture sensation. Whisker motion signals are picked up by sensory receptors—the terminations of trigeminal ganglion cells— that convert mechanical energy in the follicle into trains of action potentials. After synaptic relays in the trigeminal nuclei of the brain stem and in the thalamus, signals reach the somatosensory region of the cerebral cortex [3]. The somatosensory cortex contains a set of neuronal populations called “barrels,” each barrel responsible for processing the input from one whisker. Due to their grid-like arrangement, the whiskers can be labeled like cells in a spreadsheet (i.e., A1, C4, E2, etc). Adjacent whiskers project to adjacent barrels, so the barrel field forms an isometric map of the whiskers [4] and assumes the same labeling. Thus, for example, the several thousand neurons in barrel C3 are excited primarily by movement of whisker C3 (and much less by nearby whiskers, like C2 and C4). Neuronal activity within the barrel field is critical to the sensation of texture [2,5]. Though all investigators agree that texture sensation begins with whisker motion, two hypotheses compete to explain which features of whisker motion vary according to texture. The “resonance hypothesis” argues that textures are converted to a spatial code distributed across the whisker pad on the snout. Whisker length increases systematically from the front to the back of the rat’s snout [6,7]. Mechanical resonance frequency increases with whisker length, so there is a spatial gradient in frequency tuning of whiskers from the front to the back of the snout [7]. According to the resonance hypothesis, whisker motion across a given texture drives mechanical resonance specifically in those whiskers that possess the resonance frequencies best matching the texture’s spatial frequency [8,9]. Thus, the full set of shortto-long whiskers separates textures in the same way that the cochlea—a frequency analyzer par excellence—separates tones. Then, the map-like projection from whiskers to cortex causes each texture to excite a specific subset of barrels. In the resonance hypothesis, the spatial pattern of activity in the barrel cortex encodes the spatial frequency spectrum of the contacted texture. The “kinetic signature hypothesis” views resonance as an unavoidable consequence of the whisker structure (a tapered elastic beam), but irrelevant for the sensation of texture. This view stresses the conversion of surface shape into precisely timed motion events by individual whiskers [10]. All the whiskers that touch a texture transmit information, and texture identity is encoded by the magnitude and temporal pattern of high and low velocity whisker events [10,11]. This movement profile—the texture’s kinetic signature—is determined by surface features like the size of grains and the distance between them. Sensory receptor neurons respond to the most prominent features of the signature—the high velocity jumps over texture grains—and texture-specific firing rates and firing patterns are transmitted to barrel cortex [10]. In a new study published in PLoS Biology, Jason Wolfe et al. carried out innovative experiments aimed at selecting between these hypotheses [12]. They trained rats to whisk against sandpapers of different grain size while recording whisker motion with a linear array of optic sensors (Figure 1). When whiskers were not touching a texture but freely moving in air, their motion was continuous and smooth. But moving along the texture, their trajectory was characterized by an irregular, skipping motion: the whisker tip tended to get