Coding of modified body schema during tool use by macaque postcentral neurones

“Expansion of near space Neurophysiological and neuropsychological studies have shown that near space representations can be dynamically expanded (e.g., Fogassi et al., 1996; Iriki et al. 1996).”

“However, it would be unlikely that it would take a sudden leap in relevance when it crosses the ~70 cm line that is reachable space, where a boundary of peripersonal space is often considered to be (e.g. Iriki et al. 1996; Previc 1998; Witt et al. 2005).”

“They thus play an important role in tool use [2, 39].”

“Therefore, in agreement with both neurophysiological and neuropsychological findings (Iriki et al., 1996; Maravita et al., 2002a, 2002b) these results suggested that plastic modifications of the body schema (Head and Holmes, 1911) require the tool to be actively involved in a task.”

“Work on primate tool use (Iriki et al. 1996) suggests that several independent visuotactile representations might be stored concurrently.”

“Melville 1851), philosophy (Lotze 1885), neurology (Head and Holmes 1911), sociology (McLuhan 1964), and neuroscience (Iriki et al. 1996).”

“In the monkey, it has been shown that the area of visual receptive fields (vRFs) of bimodal visuo-tactile parietal neurons (known to map the subject’s peripersonal space) can be modified by actions per­ formed with tools (Iriki et al., 1996; Ishibashi et al., 2000).”

“For example, in Iriki and colleagues' (Iriki et al., 1996b, 2001; Obayashi et al., 2000) studies of tool-use the nature of the visual stimuli, and the spatial distribution of those visual stimuli, need to be considered in relation to the nature and distribution of the neuronal responses.”

“Although areas 2, 5, and SII do not receive strong visual input [but see [20,59]], they are reciprocally connected to multisensory areas such as the ventral premotor cortex [60,61,62], area 7 in the inferior parietal cortex [51,52,63,64], and the ventral intraparietal area [VIP; [65,66,67]], all of which are known to…”

“This is important because it is commonly assumed that pain is not referred to external objects, which is in contrast to touch touch can be referred to the tips of tools for example [27].”

“extensions and re-mappings of the body have been reported by others [19]–[21].”

“The point is nicely illustrated by research conducted on tool use (Iriki et al., 1996), which has provided a springboard for embodied cognition theorists to study the many ways in which humans couple with cultural artefacts or pieces of technological wetware so as to enhance or augment their cognitive, motor and perce…”

“…modalities exhibit plasticity, including somatosensory (Merzenich et al., 1983; Mogilner et al., 1993; Ramachandran, 1993; Manger et al., 1996), visual (Wiesel and Hubel, 1963; Cohen et al., 1997; Thaler et al., 2011) and more complex modalities such as extended-mind tools (Iriki et al., 1996).”

“There are effects measurable in terms of neurological differences, for instance in terms of an alteration of neural activity in receptive fields (e.g., [30]).”

“…representations with bimodal neurons characterized by visual receptive fields near the tactile ones (Jones et al. 1978; Colby and Duhamel 1991; Iriki et al. 1996; Duhamel et al. 1998) and to be connected with the premotor cortex (Matelli et al. 1998; Luppino et al. 1999; Lewis and Van Essen…”

“Evidence for the extension of multisensory peripersonal space by tool use has come from single unit recordings in macaque monkeys (Iriki et al. 1996a, 2001), spatial modulations of deWcits in human neuropsyhological patients (Ackroyd et al. 2002; Berti and Frassinetti 2000; Bonifazi et al. 2007;…”

“For example, experience with using a tool to achieve a goal in a normally-unreachable location can lead to a rapid extension of the PPS representation to include the area around the tip of the tool (e.g. Farnè & Làdavas, 2000; Iriki, Tanaka & Iwamura, 1996).”

“Such expansion is not observed when tools are merely manipulated, only when they are actively used to accomplish an intentional action (retrieval of food) (Iriki et al., 1996).”

“The key question is whether real objects interfere with attention because they afford grasping (Gallivan et al., 2009; Iriki et al., 1996; Mountcastle et al., 1975) or whether they require more detailed and richer visual processing (and incongruence in the visual domain results in greater competition).”

“, 2000), superior parietal lobule (Iriki et al., 1996), and inferior parietal lobule (IPL) (Fogassi et al.”

“Astonishingly, the visual receptive fields of roughly 30% of the cells had expanded to encompass the space along the length and immediately surrounding the rake (Iriki et al., 1996).”

“In the present study we investigated the effects of a special tool, the wheelchair, in extending the action possibilities of the whole body.”

“…of those bimodal neurons are arm-centered (Graziano et al., 1994) and surprisingly, following repetitive reaching tasks performed with a rake, increase to cover the expanded range of action of the hand wielding the rake, or increase to encompass the whole length of the tool (Iriki et al., 1996).”

“…previous studies (Magosso et al., 2010b) are compatible with neurophysiological results in monkeys showing that hand-centered visual RFs of neurons located in the intraparietal sulcus elongated after that monkeys used a rake to retrieve pieces of food placed in the far space (Iriki et al., 1996).”

“Vonly, E1 (%) V+P sync (%) Vonly, sync (%) Vonly, async (%) Monkey M S1 Excited 1 (2) 44 (73) 31 (50) 1 (2) Inhibited 3 (4) 0 0 3 (4) M1 Excited 5 (6) 64 (79) 51 (63) 2 (2) Inhibited 5 (6) 5 (6) 6 (7) 2 (2) Monkey N S1 Excited — 5 (33) 5 (33) 1 (6) Inhibited — 0 1 (6) 1 (6) M1 Excited — 9 (26) 8 (24) 1 (3) Inhibited —…”

“Interestingly, evidence from monkey physiology (Iriki et al., 1996), human psychophysics (Maravita et al., 2002) and human neuropsychology (Berti and Frassinetti, 2000) shows that tool usage dynamically modifies the brain's internal “body schema”, a representation of posture and positioning in…”

“Finally, it was also shown that tools may be integrated into the ‘‘body schema’’ at the neuronal level (Iriki et al., 1996; Maravita et al., 2003).”

“…the multi-sensory matching of vestibular, visual, and tactile information for the full-body, similar to visuo-tactile bimodal neurons in the premotor and intraparietal sulcus that are anchored to body parts, including the hand (Iriki et al., 1996; Graziano et al., 2000; Maravita and Iriki, 2004).”

“This idea is consistent with evidence from monkey physiology (Iriki et al. 1996), human psychophysics (Maravita et al.”

“Since Iriki’s seminal work with monkeys (e.g., Iriki et al., 1996), neuroscientific studies with humans have revealed that active tooluse can change the representation of space, in particular inducing an extension of the near space (Berlucchi and Aglioti, 1997; Berti and Frassinetti, 2000; Maravita…”

“These results have been found in multiple studies using diverse methods ranging from single cell recording, lesion case studies, neural imaging, and TMS (Iriki et al., 1996; Halligan and Marshall, 1991; Berti and Frassinetti, 2000).”

“Recent studies [11,19] have shown that peripersonal space is not activated by a simple movement executed by the hand, but only by a specific movement aimed at reaching objects in the space.”

“[11] Conceivably, the introduction of the rake could be contributing to the observed parietal modulation, because the neurons could cover a wider region of space due to wider receptive field.”

“Since the seminal work of Atsushi Iriki on macaques [38], many different studies demonstrated that, after a successful training, a proximal tool (first-order mediated action) is incorporated in the bodily experience of the subject [39-42].”

“These observations are not surprising as numerous experiments have shown that body representation in the human brain 15,32 or primates 33 modulates to incorporate additional limbs 34 , prosthetic limbs 35,36 , tools 37 , or virtual limbs 18,38–40 .”

“Beyond reaching, in PEa neural activity encodes information relevant to the subjective body image and its extension through tool use (Iriki et al., 1996; Obayashi et al., 2000; Iriki and Taoka, 2012).”

“…of this finding with respect to the existence of neuronal populations containing multisensory receptive fields that encompass a large portion of the body is compatible with neurophysiological data (Rizzolatti et al., 1981a,b; Fogassi et al., 1996; Iwamura, 1998; Graziano and Gandhi, 2000).”

“ORIGINAL RESEARCH ARTICLE published: 30 May 2014 doi: 10.3389/fpsyg.2014.00492 Tool use imagery triggers tool incorporation in the body schema”

“Visual receptive fields that generally encompass only peripersonal space are extended to include the space reachable by a physical tool [10].”

“General Discussion and Conclusion Iriki et al. (1996) and Berti and Frassinetti (2000) showed that space coding is not related in an absolute way to the coding of the reaching distance but that the activation of near and far space representation also is influenced by actions that modify the spatial…”

“…object construction (Chafee et al., 2005, 2007; Crowe et al., 2008), analysis and solution of visual mazes (Crowe et al., 2004a, 2005), tool use (Iriki et al., 1996), and interception of moving targets (Merchant et al., 2003), which can benefit from input signals conveyed by the…”

“The phenomenon describing the extension of the body representation to include non-corporeal objects in the peripersonal space, such as tools or prosthetic devices, has been extensively reported in the literature [4, 5, 6, 7], and lies also at the center of this article.”

“Importantly, such incorporation is seen only for the functional part of a tool 57 and a tool must be actively controlled for assimilation to occur 55,58 ​ .”

“…must have similar computational properties to the body schema in order to be integrated with it, at least temporarily in the course of the task (Iriki et al., 1996); (2) the recognition of crucial “affordances,” such as the fact that the food and the long stick are unreachable and the short…”

“Neurophysiological and neuropsychological studies have shown that it can expand around tools (Berti and Frassinetti, 2000; Giglia et al., 2015; Holmes, 2012; Iriki et al., 1996; Maravita et al., 2002; Maravita and Iriki, 2004) or fake arms (Blanke et al.”

“1992), the intraparietal areas (Colby et al. 1993; Iriki et al. 1996; Graziano et al. 2000), the inferior parietal areas (Leinonen et al.”

“spatial embodiment, and the plasticity of body representation following tool use, which involves motor embodiment The incorporation of a tool into the body and the expansion of peripersonal space are similar in that they seem to be due changes in the body schema (Iriki et al., 1996; Maravita and Iriki, 2004).”

“Available online on ScienceDirect (www.sciencedirect.com). colleagues had macaques reach a piece of food which was placed either outside their arm reach space (e.g. Iriki et al., 1996), or within their arm reach but occluded from their direct sight (Iriki et al., 2001).”

“, or like those that underlie the expansion of visual receptive fields during skilled tool use”