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Somatosensory Processing Subserving Perception and Action BEHAVIORAL AND BRAIN SCIENCES (2007) 30, 189–239 Printed in the United States of America DOI: 10.1017/S0140525X07001392 Somatosensory processes subserving perception and action H. Chris Dijkerman Department of Experimental Psychology, Helmholtz Research Institute, Utrecht University, 3584 CS Utrecht, The Netherlands [email protected] Edward H. F. de Haan Department of Experimental Psychology, Helmholtz Research Institute, Utrecht University, 3584 CS Utrecht, The Netherlands [email protected] Abstract: The functions of the somatosensory system are multiple. We use tactile input to localize and experience the various qualities of touch, and proprioceptive information to determine the position of different parts of the body with respect to each other, which provides fundamental information for action. Further, tactile exploration of the characteristics of external objects can result in conscious perceptual experience and stimulus or object recognition. Neuroanatomical studies suggest parallel processing as well as serial processing within the cerebral somatosensory system that reflect these separate functions, with one processing stream terminating in the posterior parietal cortex (PPC), and the other terminating in the insula. We suggest that, analogously to the organisation of the visual system, somatosensory processing for the guidance of action can be dissociated from the processing that leads to perception and memory. In addition, we find a second division between tactile information processing about external targets in service of object recognition and tactile information processing related to the body itself. We suggest the posterior parietal cortex subserves both perception and action, whereas the insula principally subserves perceptual recognition and learning. Keywords: body image; body schema; crossmodal; insula; parietal; proprioception; tactile object recognition 1. Introduction whereas early processing in the APC is mainly concerned with relatively simple features such as stimulus location The somatosensory system is involved in many aspects of and duration, subsequent processing involves detection our behaviour. It provides information about the position of the direction and velocity of a target moving over the of different parts of the body with respect to one body surface. Higher association areas combine these fea- another. It allows characterisation and localisation of touch, tures to provide information about the shape of an object stroking, and pain, and it is important for all motor or integrate it in a representation of the body. action involving the body and limbs. Furthermore, tactile Our starting point when developing this model was the exploration informs us about the characteristics of external idea that the anatomical and physiological organisation of objects, resulting in a conscious perceptual experience of the somatosensory system should reflect the eventual use the stimulus which may lead to object recognition. The of the somatosensory information rather than the detail central question addressed in this review is how cortical of stimulus characteristics. This idea has been proposed somatosensory processing is organised to subserve these previously for the visual system (Goodale & Milner different functions. 1992; Jeannerod & Rossetti 1993; Milner & Goodale We present a model that specifies the separable func- 1995). An important aspect of this model of visual cortical tional entities and their neuroanatomical correlates processing is that, in addition to describing the function of (Fig. 1). We suggest that separate cortical processing certain brain regions in terms of the perceptual character- streams exist. One projects from the anterior parietal istics (e.g., spatial or object-centred), it is just as important cortex (APC) (Brodmann areas 3a, 3b, 1, and 2) via the sec- to state the way in which we use this information (e.g., to ondary somatosensory cortex (SII) to the posterior insula, store for later recognition or to program a motor action). whereas the second terminates in the posterior parietal We suggest that a similar approach would be useful cortex (PPC). We propose that action-related processing when describing the processing characteristics of the occurs mainly in the PPC, whereas recognition and somatosensory system. perception involve the insula, as well as the PPC. The Mishkin and colleagues have described a pathway of model also distinguishes between somatosensory proces- higher cortical somatosensory processing running from sing about the body (where you have been touched) and the APC via the SII to the posterior insula and subserving about external stimuli (e.g., surface features of objects). perceptual learning and memory (Friedman et al. 1986; This distinction is reflected in largely separate bodies of Mishkin 1979; Murray & Mishkin 1984; Pons et al. literature. A final characteristic of the model is the pro- 1987), and they have suggested that this pathway might gressive integration of different stimulus features. Thus, be conceptualised as a somatosensory equivalent of the # 2007 Cambridge University Press 0140-525x/07 $40.00 189 Dijkerman & de Haan: Somatosensory processes subserving perception and action visual ventral stream (Mishkin 1979). We have incorpor- incorporates a large body of the currently available evi- ated this proposed pathway in our model, but have dence, from which testable hypotheses can be derived. expanded the neural mechanisms involved in tactile object perception to include the PPC, based on more recent patient and functional imaging studies. In addition, 2. Feature processing in the anterior parietal we suggest that the posterior insula plays a role in the per- cortex ceptual representation of the body. A third source of inspiration about the functional organ- The main processing pathways of the somatosensory isation of the somatosensory system has been the work on system from peripheral receptors to the cortex that are different body representations. The idea of a body schema concerned with touch and proprioception are well as an internal representation for action and a body image known. Input from peripheral receptors ascends through involved in perceptual identification of body features, as the dorsal column in the spinal cord and subsequently described by Paillard (1999), was particularly important. arrives in the medulla. The fibres then decussate in the The studies of patients with residual tactile processing medial lemniscus and terminate in the ventral posterior for action without perceptual awareness, as reported by lateral nucleus (VPL) of the thalamus (Martin & Jessell Paillard et al. (1983) and Rossetti et al. (2001) were 1991; Mountcastle 1984). In addition, there are projec- especially relevant. tions to the ventral posterior inferior nucleus (VPI) and Taking these sources together, this article incorporates the posterior nuclei group of the thalamus (Mountcastle existing ideas about the organisation of the cortical somato- 1984). A second ascending system, the anterolateral sensory system into one coherent model. In the following system, mainly deals with thermal and noxious stimuli, sections, we review evidence for this model in more detail. but also relays some pressure information. The antero- First, in section 2, we describe the characteristics of lateral system also projects to the VPL in addition to processing in the anterior parietal cortex (APC). Higher- smaller projections to VPI and centromedian (CM)/para- order somatosensory processing is the focus of the next, fascicular complex and the intralaminar nuclei (Berkley section 3; after which, evidence for separate processing 1980; De Vito & Simmons 1976; Sinclair 1981). for perception and action in healthy individuals is Most somatosensory information enters the cerebral described in section 4. Similarities and differences cortex through projections from the VPL to the anterior between the cortical somatosensory system and other parietal cortex (APC) (Jones & Powell 1970; Jones et al. sensory modalities are discussed in the following section, 1979; Whitsel et al. 1978). This area was originally referred 5, while crossmodal interactions form the final topic to as the first somatosensory cortex (SI), but more recently (section 6). Our intention is to provide a model that it has been suggested that only Brodmann area (BA) 3b can be considered to be the homologue of the primary area SI in non-primates (Kaas 1983; 2004). In addition, there are projections from the ventroposterior superior CHRIS DIJKERMAN is a Senior Lecturer at the Depart- nucleus (VPS) to areas 3a and 2 (Cusick et al. 1985). ment of Experimental Psychology at Utrecht Univer- Finally, small projections exist between the VPL and sity. He completed his DPhil in Psychology at the other thalamic nuclei to the secondary somatosensory University of Oxford under supervision of Larry Wei- cortex (SII), the posterior parietal and insular cortex skrantz and Faraneh Vargha-Khadem and sub- (Burton & Jones 1976; Friedman & Murray 1986; Jones sequently worked as a postdoctoral research fellow et al. 1979; Whitsel & Petrucelli 1969). with David Milner at the University of St. Andrews. His research interests include the neuropsychology of The organisation of the APC can be characterised by perceptual and sensorimotor processing, hemispatial several principles. First, it consists of four different Brod- neglect and motor imagery. He has (co)authored mann areas, BAs 1, 2, 3a, and 3b, containing several somato- more than 30 scientific papers
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