Is That Near My Hand? Multisensory Representation of Peripersonal Space in Human Intraparietal Sulcus

Abstract

Our ability to interact with the immediate surroundings depends not only on an adequate representation of external space but also on our ability to represent the location of objects with respect to our own body and especially to our hands. Indeed, electrophysiological studies in monkeys revealed multimodal neurons with spatially corresponding tactile and visual receptive fields in a number of brain areas, suggesting a representation of visual peripersonal space with respect to the body. In this functional magnetic resonance imaging study, we localized areas in human intraparietal sulcus (IPS) and lateral occipital complex (LOC) that represent nearby visual space with respect to the hands (perihand space), by contrasting the response to a ball moving near-to versus far-from the hands. Furthermore, by independently manipulating sensory information about the hand, in the visual (using a dummy hand) and proprioceptive domains (by changing the unseen hand position), we determined the sensory contributions to the representation of hand-centered space. In the posterior IPS, the visual contribution was dominant, overriding proprioceptive information. Surprisingly, regions within LOC also displayed visually dominant, hand-related activation. In contrast, the anterior IPS was characterized by a proprioceptive representation of the hand, as well as showing tactile hand-specific activation, suggesting a homology with monkey parietal hand-centered areas. We therefore suggest that, whereas cortical regions within the posterior IPS and LOC represent hand-centered space in a predominantly visual manner, the anterior IPS uses multisensory information in representing perihand space.

Bodily ownership and self-location: Components of bodily self-consciousness

“…the arm, face, and torso), while other neurons have larger multisensory receptive fields, covering even a whole hemisoma. Petkova and colleagues suggest that clusters of activation in the vPMc (and the PPc) reflect a homologous multisensory integration system in the human brain, in agreement with previous neuroimaging evidence (Bremmer et al, 2001;Brozzoli, Gentile, Petkova, & Ehrsson, 2011;Cardini et al, 2011;Makin et al, 2007;Serino, Canzoneri, & Avenanti, 2011). In addition, other studies from the same group suggested that multisensory integration in the vPMc is not only involved in the multisensory integration of body-related stimuli, but is also responsible for illusory ownership of body parts (Brozzoli, Gentile, & Ehrsson, 2012;Ehrsson, Holmes, & Passingham, 2005;Ehrsson, Spence, & Passingham, 2004;Makin, Holmes, & Ehrsson, 2008).…”

“…We then move on to a more detailed comparison of the brain structures involved. In doing so, we provide a tentative synthesis, merging the functional and anatomical data from these two studies with previous models thought to account for ownership of isolated body parts (Ehrsson, 2012;Makin, Holmes, & Zohary, 2007;Tsakiris, 2010) and self-location (Blanke & Arzy, 2005;Blanke & Metzinger, 2009). …”

Detecting peripersonal space: The promising role of ultrasonics

“…Such wide CBF modulations are in keeping with previous works indicating the activation of frontoparietal networks where the integration of sensory feedforward and feedback signals (including tactile, visual, and auditory stimuli provided near the body) related to the motor task demand and the surrounding environment occurs (Bremmer et al., 2001; Duhamel, Bremmer, Ben Hamed, & Graf, 1997; Graziano & Cooke, 2006; Graziano, Yap, & Gross, 1994; Gritsenko, Yakovenko, & Kalaska, 2009; Makin et al., 2007; Medendorp, 2011; Rizzolatti et al., 1981; Serino, Canzoneri, & Avenanti, 2011). These networks are functionally separated from that controlling the extrapersonal space, as suggested by control experiment (ii) results.…”

“…PPS representation is made of multisensory, body part‐centered reference frames, so to elaborate automated or finalized motor responses to the surrounding stimuli (Bourgeois & Coello, 2012). Wide frontoparietal networks allow integrating multisensory information within the PPS in monkeys and humans (Bremmer et al., 2001; Di Pellegrino, Ladavas, & Farné, 1997; Graziano, Taylor, & Moore, 2002; Làdavas & Serino, 2008; Makin, Holmes, & Zohary, 2007; di Pellegrino & Làdavas, 2015; Rizzolatti, Fadiga, Fogassi, & Gallese, 1997; Rizzolatti, Scandolara, Matelli, & Gentilucci, 1981; Sambo & Forster, 2009; Spence, Pavani, Maravita, & Holmes, 2008). Such a PPS representation has also a motor function, that is, it links together the instantaneous multisensory representation of PPS with the pertinent potential motor acts (Bourgeois & Coello, 2012; Cooke, Taylor, Moore, & Graziano, 2003; di Pellegrino & Làdavas, 2015).…”

“…Innovative electrophysiological and neuroimaging approaches have highlighted the involvement of large‐scale cortical networks within frontal and parietal cortices by exploring cerebral hemodynamics through cerebral blood flow (CBF), metabolic rate, and oxygenation (Bartolo et al., 2014; Cléry, Guipponi, Wardak, & Ben Hamed, 2015; di Pellegrino & Làdavas, 2015). Altogether, these measures showed significant changes in response to cognitive and motor tasks related to PPS (Brozzoli, Makin, Cardinali, Holmes, & Farnè, 2012; Coello & Fischer, 2015; Costantini, Ambrosini, Scorolli, & Borghi, 2011; Longo & Lourenco, 2007; Makin et al., 2007; Maranesi, Bonini, & Fogassi, 2014). The role and functionalities of defensive PPS have been extensively explored using motor tasks aimed at perturbing PPS (Bisio et al., 2017; Sambo, Forster, Williams, & Iannetti, 2012; Sambo & Iannetti, 2013; Sambo, Liang, Cruccu, & Iannetti, 2012).…”