Systems Neuroscience of Touch

• Prof. Ehud Ahissar, Department of Neurobiology, The Weizmann Institute, Rehovot

• Dr. Namrata Shinde, Department of Neurobiology, The Weizmann Institute, Rehovot

• Dr. Sebastian Haidarliu, Department of Neurobiology, The Weizmann Institute, Rehovot

Systems neuroscience attempts to understand the realization of brain-related functions at the level of organization that can be captured by logico-mathematical models (Von Bertalanffy, 1950), such as those describing man-made systems. In the case of perceptual systems, like that of touch, this level of organization is captured by schemes such as the one in Figure 1. Research groups addressing vibrissal touch are trying to map the vibrissal system anatomically, reveal the physiological properties of its components and the interactions between the components, and understand the function of each component and sub-system. As a result, an understanding of the emergence of tactile perception in this system is expected to arise. Importantly, systems neuroscience is not a reductionist method and its application does not preclude the value of explanations at other levels of research.

Figure 1: Major motor-sensory-motor connections in the rodent vibrissal system. Sensory information from follicle/whisker complex is transmitted via multiple pathways through the sensory regions of the brain, feeding motor subcircuits of the neocortex, cerebellum, midbrain and brainstem, which in turn feed back to the muscles that move the whiskers. Oval circles indicate the brain regions involved in vibrissal sensory-motor processing (TG, trigeminal ganglion; TN, trigeminal brainstem nuclei; RN, red nucleus; VPMdm and VPMvl, ventroposteromedial complex of the thalamus; SI, primary (barrel) somatosensory cortex; SII, secondary somatosensory cortex; ZI, zona incerta; VL, ventrolateral thalamic nucleus; MCx, motor cortex; BG, basal ganglia; Cer, cerebellum; Pn, pontine nuclei; IO, inferior olive; SC, superior colliculus; POm, posteromedial thalamic nucleus; RF, brainstem reticular formation (primarily, gigantocellular reticular nucleus, raphe magnus nucleus, supratrigeminal region); FN, facial nucleus). Black lines connecting brain regions indicate anatomical connections. Arrows indicate the direction of information flow between brain regions. Connections not labeled with arrows are reciprocal. (We thank Naama Rubin for her help in preparing the figures.)

The rodent vibrissal-touch system

The rodent vibrissal system is arguably the leading choice for systems neuroscientists addressing touch. This system offers outstanding experimental traceability at all relevant levels. At the level of whisker-object interactions the accuracy of tracking of whisker motion is at the level of the movement evoked by a single motor spike (Herfst and Brecht, 2008; Simony et al., 2010), accuracy unparalleled by any other mammalian sensory system. Clear anatomical layout allows tracing and manipulating activity in every major pathway at all levels between the sensory organ and the cortex. Importantly, rodents can perceive their environment via single whiskers, and the circuits related to single whiskers can be delineated with high confidence in many of the major stations. This combination addresses one of the largest obstacles of systems neuroscience, the sampling problem: It makes possible the tracing of a substantial portion of the neurons that are relevant to the accomplishment of a specific tactile task.

Every whisker is controlled by several intrinsic and extrinsic muscles (Hill et al., 2008; Haidarliu et al., 2010; Simony et al., 2010), and is equipped with several thousand mechano-receptors that sense the whisker's motion as well as its contacts with external objects (Ebara et al., 2002). This motor-sensory organ is equipped with mechanisms enabling it to sense specific features of the environment (Vibrissa mechanical properties). While the scope and specificity of these features is not yet known, specific mechanisms enabling the sensation of specific features have been mapped out. Salient examples are the coordinates of object location (Vibrissal location coding) and the texture of objects' surface (Vibrissal texture decoding). A common denominator of these mechanisms is their motor-sensory nature, or, more accurately, motor-object-sensory nature. That is, sensation is based on active probing of the environment by sensor motion, the result of which is received by the follicle's mechanoreceptors. Tactile perception, thus, must be based on the interpretation of the relationships between motor and sensory signals, relationships that are determined by the touched object and thus represent it (Bagdasarian et al., 2013).

The primate finger-touch system

Figure 2: Major motor-sensory-motor connections in the primate hand tactile system. Sensory information from the skin of the primate fingers is transmitted via multiple pathways through the sensory regions of the brain, feeding motor subcircuits of the neocortex, cerebellum, midbrain and spinal cord, which in turn feed back to the muscles that move the fingers. Oval circles indicate the brain regions involved in the hand tactile sensory-motor processing (DrG, Dorsal root ganglion; DH, dorsal horn of the spinal cord; Cu, nucleus cuneatus; Gr, nucleus gracilis; SC, superior colliculus; ZI, zona incerta; VPL, ventral posterolateral thalamic nucleus; IL, intralaminar nuclei of thalamus; P, posterior nuclear group of thalamus ; VL, ventrolateral thalamic nucleus; SI, primary somatosensory cortex; SII, secondary somatosensory cortex; MCx, motor cortex; BG, basal ganglia; RN, red nucleus; Cer, cerebellum; IO, inferior olive; RF, reticular formation; VH, ventral horn of the spinal cord). Other details are similar to those in Figure 1.

Tactile perception in primates is typically mediated via hand and finger movements (Lederman and Klatzky, 1987; Sathian, 1989; Turvey, 1996; Cascio and Sathian, 2001; Gamzu and Ahissar, 2001). The anatomical structure of the related sensory and motor pathways resembles that of the vibrissal system (Jones and Powell, 1969a, b; Loeb et al., 1990; Kaas, 2004) (Figure 2). Interestingly, whenever compared primates and rodents were found to exhibit comparable tactile acuities (Carvell and Simons, 1995; Horev et al., 2011; Saig et al., 2012). Although it is widely agreed that perceiving objects via touch is an active process, there is no agreement about the way in which active touch is implemented. Mainly, it is not agreed whether scanning movements are there merely to activate receptors or that the exact pattern of movements is an inherent component of perception (Connor and Johnson, 1992; Johnson and Hsiao, 1994; Gamzu and Ahissar, 2001). The latter scenario entails that touch-related movements are controlled in a closed-loop form via the tactile system (Saig et al., 2012). In contrast, as receptor activation can be achieved via a wide range of movements, open-loop activation of pre-determined movements would suffice for the former scenario.

Two (among many) challenges for systems neuroscience of touch

The question whether tactile perception emerges via closed- or open-loop processing forms one of the major current challenges facing systems neuroscience of touch. Addressing this question is tricky and the key for a successful resolution probably lies in the development of accurate testable discriminatory predictions. Another major challenge facing this field is the integration of insights obtained from rodent vibrissal touch and primate finger touch into one coherent theory of mammalian tactile perception. As a future goal one should also aspire to integrate insights from mammalian and non-mammalian tactile studies into a coherent theory of touch – given the striking similarities observed across animals The World of Touch this is not an impossible task. It seems that Evidently, addressing these challenges is essential for allowing common-ground interpretations of results obtained in different experimental settings.

References

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Sponsored by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Reviewed by: Dr. Avner Wallach, University of Ottawa, Ottawa, Canada

Reviewed by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Accepted on: 2015-04-01 08:06:01 GMT