Peripersonal space in the damaged human brain

Extinction is a clinical sign following brain damage, typically the right frontal and parietal cortex. Patients are able to detect a single stimulus presented ipsi - or contra-lesionally, but fail to report the contralesional stimulus when a concurrent stimulus is presented on the ipsilesional side.

In other terms, they cannot detect contralesional stimuli under conditions of double simultaneous stimulation, thus revealing the competitive nature of this phenomenon (di Pellegrino and De Renzi 1995; de Hann et al., 2012). Several works have shown that extinction can emerge even when concurrent stimuli are presented in different sensory modalities. For instance, a visual stimulus presented near to the ipsilesional hand can extinguish a touch delivered on the contralesional hand (di Pellegrino et al., 1997). Critically, such a crossmodal visuo-tactile extinction appears to be stronger when visual stimuli are presented in near as compared to far space: less modulatory effects of vision on touch perception were indeed observed when visual stimulation was presented far from the space immediately around the patient’s hand. This phenomenon has been interpreted as a result of multisensory processes coding a PPS presentation centred on the hand (di Pellegrino et al., 1997).

Specifically, in cross-modal visual–tactile extinction paradigms, a visual stimulus administered near a given ipsilesional body part, say the hand, strongly activates the corresponding somatosensory representation of this effector. The simultaneous activation of a somatosensory representation of the left hand by a tactile stimulus and of the right hand by a visual stimulus in PPS produces an extinction of those stimuli delivered on the left hand. This is due to the fact that extinction becomes manifest when there is a competition between more than one spatial representation, resulting in a failure to report the weaker representation, i.e., that of the left hand in previous example (Lavadas, 2002). In keeping with the monkey neurophysiological findings, visual responses to stimuli presented near the patient’s hand remain anchored to the hand when it is moved to the opposite hemispace (di Pellegrino et al., 1997). This convincingly corroborates the hypothesis that visual information is processed by a mechanism that takes a specific body part as reference and congruently follows it, staying anchored to this reference when the body part changes location. That is, multisensory interactions disclosed by extinction patients’ performance arise in a body part–

centred fashion (Ladavas 2002).

A converging line of studies suggests that another body part that might be implicated in the same mechanism is the face (Lavadas et al., 1998). As for the hand, in patients with tactile extinction, visual stimulation in the space close to the ipsilesional side of the face extinguished tactile stimulation on the contralesional side to the same extent as did an ipsilesional tactile stimulus. Instead, when visual information was presented far from the face, cross -modal extinction effects resulted to be dramatically reduced (Farnè et al. 2005a). Notably, the extinction was stronger when the homologous body part has being stimulated (i.e., left + right cheeks, and left hand + right cheek) rather than non-homologous body parts (i.e., right hand + left face and right face + left hand). In spite of being near the body, visual stimuli presented close to non-homologous body parts were treated as if they were far from the body, most likely because they are far from the relevant homologous body part. This demonstrates that different spatial regions, adjacent to different body parts, are represented separately, thus revealing that PPS is organized in a modular fashion (Farnè et al. 2005a).

Paralleling the monkey neurophysiological data showing that neurons in F4 integrate touch, vision, and audition (Graziano et al., 1997a, 1997b), crossmodal interactions between touch and audition in human PPS were first reported in right brain-damaged patients (Ladavas et al., 2001). In particular, contralesional tactile extinction on the neck was stronger when acoustic stimuli were delivered close to, as compared to far from, the ipsilesional side of the head. Moreover, crossmodal audio-tactile extinction was more severe in the patients' rear space than in the front space (Farnè et al., 2002). This could perhaps indicate the former space might indeed represent the ideal space to

auditory–tactile interactions because an object approaching the head from the rear space (where vision is not available) can be perceived only through the sound or noise it produces. In contrast, an object approaching the head from the front space would mainly benefit of visual information. This different sensitivity demonstrated that different degrees of multisensory integration may occur depending upon the functional relevance of a given modality.

Solid and convincing evidence in favour of the existence of a selective representation for the space near the body in humans derives from another pathological condition following right brain hemisphere, i.e., neglect (Schenk and Karnath 2012 for a recent review). Despite the absence of any gross primary sensory impairment, patients with neglect present a peculiar reduction of response and attention to sensory events occurring in the left (contralesional) hemispace. Several studies have confirmed that the neglect syndrome can affect selectively the space near the body or far from the body, since cases of neglect restricted to PPS have been described (Berti and Frassinetti, 2000;

Beschin and Robertson, 1997; Bisiach et al., 1986; Guariglia and Antonucci, 1992; Halligan et al., 2003; Halligan and Marshall, 1991; Ortigue et al., 2006), as well as cases of neglect restricted to extrapersonal space (Coslett et al., 1993; Cowey et al., 1994, 1999; Vuilleumier et al., 1998; Ortigue et al., 2006). Incidentally, this double dissociation, analogous to that one reported in lesion studies in monkey, constitutes further support to the notion that the human brain selectively represents the two regions of space.

Continuing the human-monkey analogy, the human representation of PPS exhibits a degree of functional plasticity too. Even though typically a far visual stimulus, being outside PPS, weakly influences tactile processing, the use of tools can change the way the brain processes visual stimuli in far space. The mostly accepted idea is that the use of a tool that elongates the arm, and therefore the reaching capabilities of the body, can induce an elongation of PPS (Berti and Frassinetti, 2000;

Farnè and Làdavas 2000; Maravita et al., 2001; Maravita and Iriki 2004, however see also Holmes 2012). Objects located in far space, when repeatedly reached with the tip of a tool, may be coded as if they were near to the body and, thus, the visual information coming from those distant objects undergoes to increased interaction with tactile processing. Through tool-use it is therefore possible to functionally remap space, so that “far becomes near” (Berti and Frassinetti, 2000). In a single

when the same task was performed with a stick, used by the patient to bisect the line in a far position: in this case, her neglect was as severe as that observed in near space. This would appear to indicate that the stick, acting as an artificial extension of the patient’s body, caused the remapping of the far space into near space.

Similar results have been described in extinction patients who, compatibly with a tool -use- dependent remapping, showed changes in cross-modal extinction assessment following tool-use:

visual stimuli presented in far space induced stronger cross-modal extinction after the use of a 38-cm rake to retrieve distant objects (Farnè and Ladavas 2000; see also Bonifazi et al. 2007; Farnè et al. 2005b, 2007, see Figure 1.6). Specifically, when patients were tested for visuo-tactile extinction before tool use, immediately after a 5-min period of tool use, and after a further 5- to 10-min resting period, far visual stimulation was found to induce more severe contralesional extinction only immediately after tool use. However, such effects were ephemeral, disappearing after a few minutes of tool inactivity. In addition, while passively holding the tool is not sufficient to trigger changes in PPS, it appears that it is the functional instead of the mere physical length of a tool that can modulate the extent of PPS elongation (Farnè et al., 2005b, 2005c, Farnè and Ladavas, 2000). As a whole, these results correspond well with neurophysiological findings revealing that that definition of peri- and extrapersonal space is not demarcated a priori, but it may be derived functionally, depending on movements that allow the body to interact with objects in space.

Figure 1.6. Schematic drawings of the experimental set-up in a study to assess the s cross-modal visual–tactile. (a). The location of visual (V) and tactile (T) stimulation is indicated by arrows. Crossmodal extinction was assessed before (a) and after (c) the patient used a rake to retrieve distant fishes (b, open circles) or pointed towards them (d). The patient’s left hand was always occluded from view by a cardboard shield (shaded area). The large dotted red hand symbolically represents the extension of the reaching space of the patient’s hand. (e) Mean percentage correct detection of the left tactile stimulus in each experimental condition. (Modified from Farnè and Ladavas, 2000; adapted from Ladavas, 2002).