Plasticity of multisensory dorsal stream functions ... - IOS Press

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Restorative Neurology and Neuroscience 28 (2010) 193–205 DOI 10.3233/RNN-2010-0500 IOS Press

Plasticity of multisensory dorsal stream functions: Evidence from congenitally blind and sighted adults Katja Fiehler∗ and Frank Ro¨ sler Experimental and Biological Psychology, Philipps-University Marburg, Marburg, Germany

Abstract. The dorsal stream has been proposed to compute vision for space perception and for the control of action. However, perceiving space and guiding movements is not only based on vision but also on other sensory modalities such as proprioception and kinesthesia. Blind people who lost vision early in life provide an exceptional example to study the plasticity of dorsal stream functions. Using fMRI and psychophysical methods, action control and space perception was investigated in congenitally blind and sighted adults while performing active and passive hand movements without visual feedback. The functional imaging data showed largely overlapping activation patterns for kinesthetically guided hand movements in congenitally blind and sighted participants covering regions of the dorsal stream. In contrast to the sighted participants, congenitally blind participants additionally activated the extrastriate cortex and the auditory cortex. The psychophysical results revealed a significant correlation between proprioceptive spatial discrimination acuity of the blind and the age when they had attended an orientation and mobility training, i.e., an extensive non-visual spatial training. The earlier the blind acquired such a spatial training the more accurate and the more precise was their space perception in later life. Our findings suggest a multisensory network of movement control that develops on the basis of sensorimotor feedback rather than being under the exclusive control of vision. Thus, visual deprivation seems to result in both cross-modal and compensatory intra-modal plasticity. The present findings further imply that dorsal stream functions are shaped by non-visual spatial information during early development. Keywords: dorsal stream, kinesthesia, motor control, posterior parietal cortex, proprioception, space perception

1. Introduction When you grasp a cup of coffee you use visual information to locate the object in space and proprioceptive and tactile information to adapt the grip aperture to the handle and to adjust the grip force to the characteristics of the mug such as material and weight. Thus, a simple action as this already requires the integration of multiple senses. Localizing objects and guiding movements in space have been ascribed to the function of the dorsal visu∗ Corresponding author: Katja Fiehler, Philipps-University Marburg, Department of Experimental and Biological Psychology, Gutenbergstr. 18, D-35032 Marburg, Germany. Tel.: +49 (0)6421 2823619; Fax: +49 (0)6421 2828948; E-mail: [email protected].

al stream arising from early visual areas and projecting to the posterior parietal cortex (Ungerleider and Mishkin, 1982; Goodale and Milner, 1992). The dorsal stream plays a crucial role in real-time control of action, when visual information about location and disposition of objects has to be transformed into the coordinate frames of the effectors being used for action (vision-for-action). Visual information used for object identification is processed by the ventral stream that projects from primary visual areas to the inferotemporal cortex (vision-for-perception). Recent data, however, suggest that the crucial distinction between the dorsal and the ventral stream is not so much between action and perception but more between egocentric and allocentric spatial coding (Schenk, 2006). Rizzolatti and Matelli (2003) refined the functional role of the dorsal stream on the basis of electrophysi-

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K. Fiehler and F. Rösler / Plasticity of multisensory dorsal stream functions

Fig. 1. Schematic representation of the visual and somatosensory pathway models in human cerebral cortex. A: According to the pathway model by Goodale and Milner (1992), the ventral perceptual stream arises from early visual areas (V1 +) and projects to regions in the inferotemporal cortex. The dorsal action stream also arises from early visual areas but projects to the posterior parietal cortex (PPC). Rizzolatti and Matelli (2003) further subdivided the dorsal action stream into a dorso-dorsal and a ventro-dorsal stream subserving online control of action and action understanding, respectively. B: For the somatosensory system, a similar pathway model has been proposed by Dijkerman and de Haan (2007). The ventral perceptual stream arises in the somatosensory cortex and sends information to the posterior insula and the posterior parietal cortex. The dorsal action stream projects from the somatosensory cortex to the posterior parietal cortex.

ological data in monkeys and clinical data in humans. They segregated the dorsal stream into two anatomically and functionally distinct sub-streams. The dorsodorsal stream terminates in the superior parietal lobe and is involved in the online control of action, as proposed by Goodale and Milner (1992) for the dorsal stream as such. The ventro-dorsal stream projects to area MT and the visual areas of the inferior parietal lobe and is involved in space perception and action recognition derived from preceding motor knowledge. In contrast to the model of Goodale and Milner (1992), action and perception are assumed to be linked in the ventro-dorsal stream. Observations in patients suffering from ideomotor apraxia support the assumption of two segregated dorsal streams (e.g., Barde et al., 2007). Both models, however, focus on visually guided movements only and therefore neglect the contribution of other sensory modalities. Early work by Mishkin (1979) already suggested a somatosensory equivalent of the ventral visual stream subserving tactile learning and memory. Dijkerman and de Haan (2007) incorporated this proposed stream in their somatosensory pathway model and expanded this model to a dorsal somatosensory stream involved in the control of action. Both streams center on the somatosensory cortex and terminate in the posterior parietal cortex whereas the perceptual stream additionally projects to the posterior part of the insula (see also Fiehler et al., 2007). Figure 1 illustrates a schematic representation of the pathway models. Comparing these models, there is a common nodal point of the visual and somatosensory dorsal stream in the posterior parietal cortex. Since the posterior parietal cortex has been considered as a classic

“association” cortex that combines information from multiple senses it is likely to be an optimal candidate for multisensory processing of information in order to form a unified representation of space and to guide movements. The aim of this article is to draw attention to the non-visual processing of action. This issue has so far largely been ignored in sensorimotor control theories. First, we will give a short overview of previous findings on the visual dorsal stream. Then, we will review recent empirical evidence in sighted and congenitally blind people examining the role of the dorsal stream in non-visual control of action. Finally, we will consider developmental changes of dorsal stream functions.

2. Visual action guidance in the dorsal stream The most compelling evidence for the visual pathway model is derived from clinical studies (Goodale and Milner, 1992). Patients with lesions in the dorsal stream, in the superior parietal lobe and the intraparietal sulcus, were unable to use visual information to correctly pre-shape the hand according to the size of a graspable object (optic ataxia), although they had no problems describing the orientation and relative position of those objects (Perenin and Vighetto, 1988). Conversely, patient DF, who suffered from a bilateral damage in the ventral stream, in the ventrolateral occipital region, had no difficulty using vision for grasping or aiming at an object, although she was unable to indicate the size, shape, and orientation of an object (Goodale et al., 1991). The observation of a double


dissociation led to the idea that action and perception are mediated by separate visual streams in the cerebral cortex. Behavioral results in neurologically intact people provided additional support for the visual pathway model (for a review see Goodale and Westwood, 2004). Electrophysiological and neuroimaging studies have led to the localization of specific subregions within the dorsal and ventral streams subserving object-directed action and object recognition. Here, we want to focus on cortical regions within the dorsal stream. There is converging evidence that areas along the intraparietal sulcus play a key role in visually guided movements. Various divisions within the intraparietal sulcus of the macaque brain have been found to be involved in the control of specific effectors, including the hand (anterior intraparietal area, AIP), arms (medial intraparietal area, MIP), head (ventral intraparietal area, VIP), and eyes (lateral intraparietal area, LIP) (Colby, 1998). Putative human functional homologues of the intraparietal areas have been proposed (Grefkes and Fink, 2005), however, these results are still ambiguous. Observations in patients suffering from optic ataxia suggest a key role of the posterior parietal cortex in reaching. Especially lesions of the medial occipito-parietal junction, the intraparietal sulcus, the superior occipital gyrus, and the superior and inferior parietal lobe are commonly found in optic ataxia patients (Karnath and Perenin, 2005). Imaging studies in healthy participants also revealed reaching-related activation in the medial occipito-parietal areas and the medial intraparietal sulcus (Prado et al., 2005; Filimon et al., 2007). Activations in similar regions have been reported for pointing movements as well (Astafiev et al., 2003; Connolly et al., 2003; Fernandez-Ruiz et al., 2007). In contrast to reaching, pointing movements do not require the extension of the arm in order to touch an object. They only demand to direct the index finger towards the object. The overlapping activation foci reported for reaching and pointing might be caused by a common mechanism which processes the current movement target (Diedrichsen et al., 2005). Cortical activation of the anterior intraparietal sulcus has been consistently reported for grasping movements (Faillenot et al., 1997; Binkofski et al., 1998; Culham et al., 2003; Frey et al., 2005). Accordingly, transcranial magnetic stimulation (TMS) applied to the anterior intraparietal sulcus disrupts online hand-preshaping adjustments to sudden changes in object orientation (Tunik et al., 2005). Furthermore, lesions in the anterior intraparietal sulcus cause severe impairments in grasping while reaching remains relatively intact (Binkofski et al., 1998). While

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both grasping and reaching share the transport component of moving the hand to the object, only grasping also requires the grip component that uses information about object size and orientation. In addition to arm and hand movements, movements of the eyes play an important role in visually-guided movements. Functional magnetic resonance imaging (fMRI) reliably demonstrated saccade-related activation in the posterior half of the medial intraparietal sulcus, also called the parietal eye field (PEF), and in the superior parietal lobe (Pierrot-Deseilligny et al., 2004). The activation in area PEF can be modulated by head position (Brotchie et al., 2003), direction of a pointing movement (Medendorp et al., 2005), attention (Sereno and Maunsell, 1998), and spatial updating when gaze changes (Medendorp et al., 2003). Finally, it is important to point out that these functionally specific brain areas do not show an all-or-non response but rather a preferential response to the specific effector (Levy et al., 2007). Beyond the recruitment of effector-specific brain regions, successful performance of object-directed actions requires the computation of object attributes, such as size, shape, and orientation. In line with this view, a dorsal stream area, the lateral occipito-parietal junctions, responded systematically to object orientation (James et al., 2002; Valyear et al., 2006). Moreover, Shmuelof and Zohary (2005) reported a dissociation between dorsal and ventral fMRI activation showing that dorsal stream areas were tuned to both the visually perceived form of the grasping gesture and the object shape, whereas ventral stream areas were only sensitive to object identity.

3. Kinesthetic action guidance in the dorsal stream Kinesthesia is the perception of the motion of a body part. It is mediated by muscle spindle receptors and mechanoreceptors in the joints, tendons and skin (Matthews, 1988). Kinesthetic and other proprioceptive information from muscle receptors is mainly processed in area 3a (Phillips et al., 1971; Tanji and Wise, 1981). In area 2, the dominant input originates in the joints and muscle receptors as evidenced by single cell recording studies in monkeys (Iwamura et al., 1983; Mountcastle and Powell, 1959) and brain imaging studies in humans (Bodegard et al., 2003; Naito et al., 2005; for an overview see Burton, 2002a). Area 2 has dense cortico-cortical connections to the superior parietal lobe (Jones and Powell, 1969; Pandya and

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Fig. 2. Experimental protocol and experimental setup. A: The experimental protocol used in the fMRI experiments. Three different line patterns had to be traced with a stylus and maintained across a delay of 8 s. Then, a probe stimulus had to be traced and a motor response had to be given indicating whether the probe matched one of the stimulus from the previous stimulus set. Task stimuli presented for movement encoding contained zero (BA), one (SS1), two (SS2), or three (SS3) multi-segment line patterns and three, two, one, or zero circular line patterns, respectively. An increasing number of multi-segment line patterns led to an increase in movement difficulty. B: The experimental setup. Task stimuli were different line patterns engraved in plastic cards. The cards were attached to a triangular card holder which could be turned such that one side was oriented towards the hand of the participant. Blindfolded participants traced the line patterns with a stylus with their right hand and performed task-related button presses with their left hand. SS, set size; BA, baseline; ITI, inter-trial interval.

Kuypers, 1969) and through its connection to the anterior intraparietal area (Sakata et al., 1973) providing extensive mutual interaction between the primary somatosensory cortex and the posterior parietal cortex. Neurons in the superior parietal lobe are active during passive joint rotation and deep tissue pressure as well as during active arm movements (Mountcastle et al., 1975; Lacquaniti et al., 1995). In contrast to neurons in primary somatosensory cortex, neurons in superior parietal lobe respond to multiple joint interactions and integrate both tactile and joint information (Sakata et al., 1973) suggesting that this region is involved in higher order processing of somatosensory input. Accordingly, patients with lesions in the posterior parietal cortex suffer from tactile apraxia, a severe impairment of exploratory hand movements performed on the basis of tactile and kinesthetic input (Binkofski et al., 2001). Further support is provided by fMRI data which demonstrate activation in the human superior parietal lobe and anterior intraparietal sulcus during exploratory hand and finger movements performed without visual feedback. Binkofski and colleagues (1999a, 1999b) asked participants to manipulate complex and simple meaningless plastic objects by natural exploration movements with the goal of exploring object features. Contrasting brain activity between complex and simple manipulation showed significant activation in the anterior part of the intraparietal sulcus and in the superior parietal lobe. Activation in the superior parietal lobe and the anterior intraparietal sulcus were also observed when participants molded a previously palpated object out of plasticine (J a¨ ncke et al., 2001).

The studies reviewed so far used unconstrained hand and finger movements that differ in their quantity and quality within and across participants. Moreover, tactile and kinesthetic input signals are intermingled so that the impact of kinesthetic information on the control of action cannot be properly disentangled. In a recent fMRI study, we investigated the neural correlates of kinesthetically guided hand movements using a controlled tracing task (Fiehler et al., 2008). Participants were asked to subsequently trace three engraved line patterns with a stylus held in their right hand and to maintain the corresponding hand movements over a delay period of 8 seconds. Finally, a probe line pattern was presented and participants indicated whether that movement matched one of the previous three hand movements. In order to substantiate the impact of an observed activation pattern we systematically varied movement difficulty. Areas exhibiting increased activity in response to increased movement demands are very likely specifically involved in processing that stimulus (e.g., Druzgal and D’Esposito, 2001). The experimental protocol and the task conditions are depicted in Fig. 2. Participants were blindfolded during the experiment so that movements were primarily guided by kinesthesia. The impact of tactile information was strongly reduced by the usage of the stylus. Kinesthetically guided movements activated the primary and secondary somatosensory cortex. The main activation focus, however, was located in area 2 of the primary somatosensory cortex substantiating previous findings on kinesthetic information processing. Moreover, activation was found in the superior parietal lobe, the anteri-


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Fig. 3. Cortical activation of kinesthetic guidance of movements (encoding period) in sighted and congenitally blind participants. A: Brain activation revealed by sighted (SC) participants performing kinesthetically guided hand movements. B: Group averaged statistical parametric maps of the activation overlap between congenitally blind (CB, n = 12) and sighted control (SC, n = 12) participants. The conjunction analysis (activation of the CB group ∩ activation of the SC group) revealed significant activation in areas of the dorsal stream in both groups. C: Group-specific cortical activation. Group averaged statistical parametric maps from the between-group contrasts (two-sample t-test) yielded higher activation for sighted control (SC) than congenitally blind (CB) participants in the parieto-occipital fissure and the pre-supplementary motor area (left). Congenitally blind compared to sighted control participants showed increased activity in the auditory cortex and the extrastriate cortex (right). L, left; R, right.

or and posterior portion of the intraparietal sulcus, and the premotor cortices (Fig. 3A). These areas showed an increase of activation with increasing movement difficulty. We also observed a small activation in a brain region located in the ventral stream, in the right lateral occipital complex (LOC). Our results provide empirical evidence for the somatosensory pathway model suggesting an important role of the superior parietal lobe and the anterior intraparietal sulcus in the kinesthetic guidance of hand movements. Brain areas activated by kinesthetically guided hand movements largely overlapped with cortical regions previously reported for visually guided hand movements. This is consistent with findings in monkeys showing that neurons in the anterior intraparietal area do not only discharge during visually-guided hand shaping but also during object manipulation in the dark

based on tactile and kinesthetic input (Sakata et al., 1973; Sakata et al., 1995, for a review see Andersen et al., 1997). In summary, our results in humans suggest a modality-independent action representation system of the dorsal stream that is utilized for multisensory control of action. Studies on visuo-haptic processing of grating orientation and macrospatial shape used for guiding action strengthen the claim of multisensory functioning of the dorsal stream (for a review see Sathian and Lacey, 2007). An early positron emission tomographic (PET) study demonstrated activation in a dorsal stream region, the left parieto-occipital cortical (POC) region, when tactile discrimination of grating orientation was contrasted with a control task (Sathian et al., 1997). Area POC located near the human V6 complex is the putative equivalent to macaque area V6/PO, where a large pro-

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portion of neurons are orientation-selective (Galletti et al., 1991). Since a similar region had been reported for visual discrimination of grating orientation (Sergent et al., 1992), area POC seems to commonly process orientation information across vision and touch. In a later fMRI study, additional activation was found in the right postcentral sulcus and the left anterior intraparietal sulcus using a similar paradigm (Zhang et al., 2004). A direct comparison of activation observed during tactile and visual discrimination of the orientation of gratings revealed a common activation focus in the right intraparietal sulcus regardless of which hand was stimulated (Kitada et al., 2006). In accordance with results on shape processing in monkeys (Duhamel et al., 1998), Stilla and Sathian (2008a) reported bisensory shapeselectivity in various foci along the intraparietal sulcus. The magnitude of visually- and haptically-evoked activity was significantly correlated in the left posterior intraparietal sulcus and the right LOC, suggesting that these areas are involved in modality-independent processing of object shape. Interestingly, the right LOC activation reported by Stilla and Sathian (2008a) largely overlaps with the LOC activation found in our study (Fiehler et al., 2008). Considering the subjects’ task, it is conceivable that they tried to extract the underlying shape of the movement path in order to use this information for subsequent movement recognition. Together with findings of Amedi and colleagues (2001, 2002), the ventral stream seems not to be restricted to the visual modality, as we propose for the dorsal stream as well.

4. Plastic changes of dorsal stream functions Since movements are mainly guided by vision, the question arises whether visual experiences are indispensable for the development of dorsal stream functions. To test this hypothesis, we investigated congenitally blind adults with the same experimental protocol as described above (see Fig. 2). Brain activity of 12 congenitally blind adults was compared to a group of 12 sighted adults who were matched by age, years of education, and handedness. Both groups did not differ in their task performance. Execution of kinesthetically guided hand movements activated the bilateral primary somatosensory cortex, the left anterior intraparietal sulcus, and the left superior parietal lobe in blind participants (Fiehler et al., 2009a). The same brain regions were observed in the sighted control group as revealed by a conjunction analysis (Fig. 3B). The finding

that congenitally blind people recruited the same dorsal stream areas as the sighted implies that dorsal stream functions do emerge in the absence of visual experience. Moreover, our result demonstrates that dorsal stream activation by the control of action is not mediated by visual imagery. Our interpretation gains further support by a recent fMRI study showing overlapping activation in the ventro-dorsal stream area hMT+ for congenitally blind and sighted individuals. Area hMT+ was active during passive perception of optic and tactile flow in sighted and of tactile flow in congenitally blind participants (Ricciardi et al., 2007). Unlike the sighted, blind individuals must rely strongly on their remaining senses to guide movements. Based on previous findings, it is likely that pre-existing connections between the somatosensory cortex and the posterior parietal cortex have been strengthened in order to obtain efficient motor control on the basis of somatosensory information. Such cortical changes can be caused by physiological modification, environmental pressure, functional significance, and experience (for a review see Pascual-Leone et al., 2005). In this vein, sighted compared to blind participants elicited stronger activation in the precuneus extending into the parietooccipital fissure and in the pre-supplementary motor area (Fig. 3C). Both brain regions are part of a neural network engaged in spatially-guided behavior. While precuneus activation has been found for tactile object localization and processing of spatial coordinates (Selemon and Goldman-Rakic, 1988; Reed et al., 2005), activation in the pre-supplementary motor area is associated with higher order motor control, i.e., movement planning and preparation and processing of complex sequential movements (Picard and Strick, 1996). Since activation in the pre-supplementary motor area systematically varies with movement difficulty (Harrington et al., 2000), we suggest that the stronger activation in the sighted individuals is due to higher task-related sensorimotor demands because of less experience in nonvisual movement control. Sighted participants had to recruit more cortical resources in order to perform the kinesthetic movement task as efficiently as the blind. Blind compared to sighted participants elicited stronger activation in the extrastriate cortex and in the auditory cortex while performing kinesthetically guided hand movements (Fig. 3C). These coactivations imply both cross-modal plasticity in the visual cortex and intramodal plasticity in the auditory cortex due to visual deprivation. In the following, we will discuss the findings together with current research on neural plasticity in blind individuals.


It has been shown that visual deprivation leads to cross-modal reorganization of the occipital cortex, changing its functional and structural identity (for a review see Collignon et al., 2009; R o¨ der and Ro¨ sler, 2004; Burton, 2003). As a consequence of the afferent input changes, occipital cortex tissue can process input from other sensory modalities, such as somatosensation and audition (Schlaggar and O’Leary, 1991; Sur and Leamey, 2001). Accordingly, a number of neuroimaging studies have demonstrated task-dependent activation of the occipital cortex during tactile (e.g., Büchel, 1998; Sadato et al., 1996) and auditory (e.g., Weeks et al., 2000; Gougoux et al., 2005) tasks. Even high-level cognitive tasks like memory (Amedi et al., 2003; Ro¨ der and Ro¨ sler, 2003) and language processing (Burton et al., 2002b; R o¨ der et al., 2002) activate the visual cortex of the blind. Since transient visual deprivation in sighted humans can induce primary visual cortex activation for tactile and auditory stimulation (Merabet et al., 2008), it seems unlikely that such cross-modal plastic changes are caused by newly established cortical connections. Thus, Pascual-Leone and colleagues (2005) proposed two mechanisms that may cause cross-modal plasticity: a fast process unmasking existing connections that are normally inhibited when sight is present and a slow process strengthening preexisting connections and establishing new connection between cortices. The response of the occipital cortex in the blind may simply reflect a non-functional co-activation. Transcranial magnetic stimulation (TMS) is a useful approach to determine the functional relevance of a specific brain region for a particular behavior. Thus, this method has been applied to investigate the necessity of the visual cortex of the blind showing that TMS over visual cortices interfere with Braille reading (Kupers et al., 2007; Cohen et al., 1997), verbal processing (Amedi et al., 2004), and sound localization (Collignon et al., 2007) in the blind. Furthermore, in a recent fMRI study tactile acuity thresholds were predicted by activation magnitudes of the visual cortex (Stilla et al., 2008b). These results indicate that visual cortex activation in the blind is not an epiphenomenon but rather reflects a functional involvement of that region. In addition to cross-modal changes, the loss of vision can cause changes within primary sensory cortices. Blind Braille readers, for example, demonstrate an expanded sensorimotor representation of the Braillereading finger (Pascual-Leone and Torres, 1993), and blind individuals who use multiple fingers to read Braille showed disordered cortical somatotopy (Sterr et

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al., 1998). In our study described above, blind participants showed stronger activation of the auditory cortex compared to sighted participants. Somatosensory input to the auditory cortex has been demonstrated in human and non-human primates. Intracranial recordings in monkeys have shown activation in the caudomedial auditory cortex (CM) triggered by repetitive electrical stimulation of the median nerve (Schroeder et al., 2001), by cutaneous stimulation at the head/neck and hand, and by kinesthetic stimulation at the elbow (Fu et al., 2003). The timing and laminar activation for somatosensory and auditory inputs are nearly the same in monkey area CM supporting somatosensory-auditory integration in this area. Using fMRI, a putative human homologue of area CM has been identified (Foxe et al., 2002; Schu¨ rmann et al., 2006). Comparable to monkey area CM, this subregion of the human auditory cortex responded to both auditory and somatosensory stimuli. The activation strength was larger for multisensory than summed unisensory stimulation suggesting that this auditory region represents a multisensory convergence zone that subserves processing of composite audiotactile events. This result was confirmed by a recent electrophysiological study that demonstrated early activation of auditory cortical areas in response to vibrotactile stimulation (Caetano and Jousm a¨ ki, 2006). Thus, multisensory input signals are integrated early in the cortical processing hierarchy, i.e., in brain areas traditionally considered as unisensory. The auditory cortex activation observed in our congenitally blind participants overlaps substantially with the human equivalent of monkey area CM. We suggest that the greater experience in and stronger reliance on composite somatosensory and auditory feedback for guiding action might have led to a stronger excitability of the multisensory convergence zone in the auditory cortex in the blind. In sum, the coactivation of the extrastriate and the auditory cortices in the blind imply both cross-modal and intramodal plasticity due to visual deprivation.

5. Developmental changes of dorsal stream functions Recent findings in animals (Wallace et al., 2004; Carriere et al., 2007) and humans (R o¨ der et al., 2007; Putzar et al., 2007) clearly emphasise the role of sensory experiences during the first months of life for the development of multisensory perception and action control. It has been shown that multisensory neurons and

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multisensory integration in a number of brainstem and cortical sites of the cat and monkey develop comparatively late in ontogeny and thus require a considerable period of postnatal maturation (Wallace and Stein, 2000; Wallace et al., 2006). For subcortical structures, this maturation process appears to be gated by the appearance of functional projections from the association cortex (Wallace, 2004). As a consequence, the development of multisensory integration significantly depends on early sensory experience. In support of this, eliminating the visual sense after birth causes substantial impairments of the integrative capabilities of multisensory neurons in the cat resulting in a decreased sensitivity to cross-modal events (Wallace et al., 2004; Carriere et al., 2007). In line with the findings in animals, developmental studies in children suggest that multisensory functions evolve during the first years of life (Lewkowicz and Lickliter, 1994). This assumption has recently gained further support. Putzar et al. (2007) investigated humans who experienced early visual deprivation during the first months of life as a result of binocular cataract. Using a multisensory interference task, cataract patients showed reduced audio-visual interactions compared to healthy controls. This result provides additional evidence that normal vision during the first months of life may be critical for the full development of cross-modal perceptual functions. Accordingly, impaired multisensory interactions have been found in congenitally blind people as well (H o¨ tting et al., 2004). The impact of sensory experience during ontogeny on dorsal stream functions, i.e., space perception and control of action, has so far been studied only sparsely. Results of an intriguing experiment by R o¨ der et al. (2007) suggest that the availability of early visual input determines the spatial reference frame used for multisensory control of action. Congenitally blind, late blind and sighted participants were asked to perform an auditory version of a spatial congruency task. Based on the result pattern, the authors suggest that sighted and late blind people preferentially rely on an objectcentered external reference frame (i.e., the sound was located on the basis of a Cartesian coordinate system), whereas congenitally blind people preferentially use a body-centered internal reference frame (e.g., the sound was located on the basis of an anatomically hand anchored coordinate system). Therefore, the development of automatic remapping of sensory inputs onto a common external reference frame seems to require visual input during ontogeny. However, it is unclear whether spatial processes once determined are insensitive to further changes or

whether they still underlie plastic changes due to early sensory experiences. To this end, we recently tested congenitally blind participants who differed in their non-visual spatial experience during ontogeny (Fiehler et al., 2009b). Early non-visual spatial experience was quantified by the age when congenitally blind participants attended an orientation and mobility training (OMT) course. The OMT is a standardized multistage education program according to the guidelines of the German society of visually impaired humans and embodied in German law (code of social law: SGB V). It includes a basic training (e.g., techniques to orient in a room, in a building, and in public by using internal and external cues) and a long cane training (Blasch et al., 1997; Brambring, 2003). In the study, participants performed a proprioceptive spatial movement task in which their right arm was passively moved along the horizontal plane and spatial judgements about the movement trajectories were required. Spatial discrimination acuity and response variability were assessed by an adaptive psychophysical procedure (Treutwein, 1995). Congenitally blind participants who attended an OMT after the age of 12 years revealed reduced sensory acuity and enhanced response variability compared to both the congenitally blind group who participated in an OMT before the age of 12 years and to a sighted control group (Fig. 4, left). The comparable task performance of congenitally blind adults with an early OMT and sighted controls implies that non-visual spatial experience can successfully compensate for the lack of vision. Proprioceptive spatial acuity and response variability significantly covaried with the age by which congenitally blind individuals acquired non-visual spatial experience via the OMT program (Fig. 4, right). The earlier blind individuals started the OMT the more accurate and the more precise was their space perception. This finding suggests that proprioceptive spatial acuity in adulthood depends on non-visual spatial experience during early development. Early sensory experience might unmask and strengthen pre-existing cortical connections or establish new ones that compensate for the lack of vision (cf., Pascual-Leone et al., 2005). The results have some practical implications encouraging instructors of schools of visually impaired people to start intense OMT as early as possible. Based on the studies reviewed above, the modalityindependent representation system of the dorsal stream (posterior parietal cortex) most likely serves as the neural basis for such non-visual spatial processes in the blind. This hypothesis gains first support by studies conducted on monkeys (e.g., Sakata et al., 1973, 1995)


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Fig. 4. The influence of age, when orientation and mobility training (OMT) was experienced, on proprioceptive-spatial acuity in adulthood. A: Group mean sensory threshold (left) with standard errors of the mean for congenitally blind participants attending an OMT before or after the age of 12 years and sighted control participants. The scatter plot of the sensory threshold against the age at OMT shows a significant correlation between the two variables (right). B: Group mean of the response variability (left) with standard errors of the mean for congenitally blind participants attending an OMT before or after the age of 12 years and sighted control participants. The scatter plot of the response variability against the age at OMT also demonstrates a significant correlation between the two variables (right). Significant group differences and correlations are marked with an asterisk.

and humans (e.g., Fiehler et al., 2008; Stilla and Sathian, 2008a) demonstrating an involvement of the posterior parietal cortex in both visual and somatosensory processing of space and action. Secondly, imaging studies suggest that the functional organization of the dorsal stream can develop in the absence of any visual experience (Fiehler et al., 2009a; Ricciardi et al., 2007). Thus, dorsal stream functions are accessible for congenitally blind, late blind and sighted individuals. Since visual cortex activation has been frequently observed in blind participants (for a recent review see Sathian and Lacey, 2007), it is conceivable that the visual cortex in addition to posterior parietal areas engages in the non-visual spatial training.

6. Conclusion Together, the reviewed results provide evidence that the action-representation system of the dorsal stream is utilized not only for visual but also for somatosensory guidance of movements. Findings in the congenitally blind further imply that dorsal stream functions also develop in the absence of visual input and can be altered by postnatal sensory experience. The availability of visual inputs during ontogeny seems to set up the final spatial reference frame used for guiding movements. However, non-visual spatial experience during the first years of life appears nevertheless to be capable of shaping spatial processing mechanisms.

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Acknowledgements This research was supported by grant Ro 529 and Fi 1567 from the German Research Foundation (DFG) assigned to Frank Ro¨ sler and Katja Fiehler and by the TransCoop-Program from the Alexander von Humboldt Foundation assigned to Katja Fiehler and Denise Y.P. Henriques.

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