Texture signals in whisker vibrations 1 Dynamic Translation of Surface Coarseness into Whisker Vibrations

Rodents in their natural environment use their whiskers to distinguish between surfaces having subtly different textures and shapes. They do so by actively sweeping their whiskers across surfaces in a rhythmic motion. To determine how textures are transformed into vibration signals in whiskers and how these vibrations are expressed in neuronal discharges, we induced active whisking in anaesthetized rats, monitored the movement of whiskers across surfaces, and concurrently recorded from trigeminal ganglion (TG) neurons. We show that tactile information is transmitted through high frequency micromotions superimposed on whisking macro-motions. Consistent with this, we find that in most TG neurons, spike activity and high frequency micro-motions are closely correlated. To determine whether these vibration signals can support texture discrimination we examined their dependence on surface roughness and find that both vibration signals carry information about surface coarseness. Despite a large variability in this translation process, different textures are translated into distinct vibrations profiles. These profiles are dependent on whiskers properties, on the radial distance of the surfaces and on whisking frequency. Using the characteristics of these signals, we employ linear discriminant analysis and find that all whiskers were able to discriminate between the different textures. This classification did not depend on whisking frequency, while deteriorating with radial distance. Finally, increasing the number of whisks and integration of tactile information from multiple whiskers improved texture discrimination. These results indicate that surface roughness is translated into distinct whisker vibration signals that result in neuronal discharges. However, due to the dynamic nature of this translation process, we propose that texture discrimination may require the integration of signals from multiple spatial and temporal sensory channels to disambiguate surface roughness. Texture signals in whisker vibrations 3 Introduction Behaviorally relevant tactile stimuli have complex spatial and temporal structures, and animals can readily perceive and discriminate among these stimuli to guide their behavior. Most of our knowledge of somatosensory function has been obtained using stimuli consisting of simple features designed to tease apart neuronal stimulus selectivity. Thus, little is known about the behavior of the somatosensory system in response to stimuli that are behaviorally relevant and are found within the animal’s natural sensory environment. The system is highly specialized for processing fine tactile information acquired by the array of whiskers, on the facial mystacial pad. Rats actively sweep their whiskers across surfaces in a rhythmic forward and backward motion with a frequency ranging from 5 to 25 Hz, called whisking, to locate and distinguish objects in the animal’s immediate sensory environment (Carvel and Simons, 1990; Sachdev et al.,2001; Berg and Kleinfeld,2003; Bermejo et al.,2002). Whisker movements excite several hundred primary afferent fibers that innervate mechanoreceptors on each whisker shaft (Ebara et al., 2002). These signals travel along the sensory nerve, to the brain stem. The axons of the brain stem neurons cross the brain midline and travel to the thalamic somatosensory nuclei. Thalamic neurons project to the primary somatosensory cortex, conveying information to layer 4 cell populations called “barrels” (Welker,1971; Woolsey and Van der Loos, 1970). Psychophysical studies have demonstrated that rats using their whiskers can reliably detect small differences in surfaces textures (Carvel and Simons, 1990, 1995; Guic-Robles et al., 1989; Ritt et al., 2008; von Heimendahl et al., 2007). Thus, the somatosensory system appears well suited for conveying and processing complex sensory information rapidly and reliably (Jones and Diamond, 1995; Diamond et al., 2008). What mechanisms might underlie this striking capacity for texture discrimination? One attractive model posits that the resonant properties of whiskers, which vary systematically with whisker length along whisker rows, will mediate texture discrimination (Brecht et al. 1997; Hartmann et al., 2003; Mehta and Kleinfeld, 2004; Kleinfeld et al., 2006; Moore and Andermann, 2005; Neimark et al., 2003). Texture signals in whisker vibrations 4 When rats actively sweep their whiskers across textured surface, the vibrissa the resonance frequency of which most closely matches the texture-induced input frequency will transmit the greatest vibrations to the follicle (Andermann et al., 2004). Different whiskers would be tuned to different frequencies and thus split the tactile vibration signals into labeled frequency lines in the cortex (Mehta and Kleinfeld, 2004; Moore and Andermann, 2005; Moore, 2004; Neimark et al., 2003; Andermann et al., 2004; Hartmann et al., 2003). An alternative view suggests that the mechanical properties of the vibrissae act to translate surface roughness into different intrinsic frequency or velocity modes in each vibrissa (Andermann et al., 2004; Hipp et al., 2006). The differences between surfaces are expressed by the extent to which different modes are favored within each vibrissa (Fend et al., 2003; Mehta and Kleinfeld, 2004). The neural representation of these modes can either be expressed in discharge probabilities that increase in proportion to stimulus velocity (Shoykhet et al. 2000; Arabzadeh et al. 2003, 2004, 2005, 2006; Jones et al., 2004) or by the preservation of the velocity profile of the vibration in the temporal pattern of spikes (Arabzadeh et al., 2006, 2005; Hipp et al., 2006; Deschenes et al., 2003; Gibson and welker, 1983a,b; Lichtenstein et al., 1990; Shoykhet et al., 2000). Recent seminal studies, using artificial whisking across textures have concluded that the velocity profile signal in whiskers transmits texture coarseness to the whisker shaft (Arbzadeh et al., 2003, 2004, 2005; Kleinfeld et al., 2006; Albarracín et al., 2006). Texture discrimination can then be achieved using cortical spike rate and patterns (Arbzadeh et al., 2006). While these studies have advanced our understanding on the representation of “natural” stimuli such as textures in the rat whisker somatosensory system, several key issues remain unresolved: What are the characteristics of texture related whisker vibrations that are transmitted to the whisker shaft? How are these vibrations translated to TG neurons discharges? Are these features able to support texture discrimination? What are the functional consequences of large variability in this translation process? To address these issues we induced artificial whisking across textures in anaesthetized rats, monitored whiskers' vibrations at the shaft, and concurrently recorded from TG neurons. We first examined how whiskers' motion along a Texture signals in whisker vibrations 5 surface is converted to discharge patterns in TG neurons. Then we characterized the texture-related whisker vibrations that underlie these discharge patterns. With the use of linear discriminant analysis (LDA) we were able to determine whether whisker vibrations are able to support texture discrimination and its dependence on intrinsic and extrinsic variables. Texture signals in whisker vibrations 6 Material and Methods