Review
Mechanisms underlying embodiment, disembodiment and loss of embodiment

https://doi.org/10.1016/j.neubiorev.2007.07.001Get rights and content

Abstract

Bodily experience is a complex, mostly unconscious, process that requires the integration of multiple sensory inputs. This paper reviews the sensory systems involved in internal representations of the body—primarily the proprioceptive, motor, vestibular, and visual systems. Various neurological disorders are defined by aberrations in bodily experience—including the perceptual ablation or disembodiment of body parts, “filling in” of amputated body parts, or reduplication of body parts. These perceptual aberrations are discussed and their implications for the central and peripheral systems involved in updating and retrieving internal representations of the body are highlighted. Bodily perception and egocentric frames of reference can be experimentally manipulated through visual capture (e.g., using rubber limbs), functional adaptation and embodiment of tools and prostheses, and changes in afferent sensory feedback (e.g., through stimulation of muscle spindles). These perceptual illusions are described, and discussed for their implications for the mechanisms underlying bodily perception.

Introduction

The ownership and embodiment of one's body is a seemingly trivial aspect of the self that is nevertheless essential for successful interaction with external objects and people. However, complex mechanisms underlie the maintenance of internal representations of the body (body schemata), body ownership and embodiment. In particular, embodiment is a complex phenomenon that extends from self-embodiment to the embodiment of habitually used tools, prostheses or rubber limbs that effectively extend or displace the normal area of influence of body parts. This paper reviews the neural and sensory mechanisms underlying bodily experience. It then defines the conceptually unique aspects of bodily experience from internal representations of the body and manifestations of the body image and body schema, to body ownership and dis-ownership, and embodiment and disembodiment. It finally reviews some of the techniques by which embodiment can be modified or manipulated; such as through tool and prosthesis use, and rubber limb illusions.

The present review suggests a model whereby embodiment operates both via automatic bottom-up and potentially conscious top-down processes; these permit the establishment, with respect to the body, of sensory–motor and motor–sensory maps of the limbs—and subsequently, tools and prostheses after amputation—whereby they may be optimally deployed in space. The account accommodates a number of otherwise disparate phenomena (such as phantom sensations, rubber limb illusions, unilateral neglect, somatoparaphrenia, and alien limb phenomena), and even suggests that the phantom limb phenomenon may play an adaptive role in certain contexts, rather than being a mere by-product of a disturbed spatial reference system.

Section snippets

Multisensory integration and egocentric frames of reference

Information regarding the body in space is generated via the integration of afferent sensory information relating to the self in space—including retinal, somaesthetic, proprioceptive, vestibular and auditory inputs—together with efferent information relating to motor output and the movement of the body in space, including movement of the eyes, neck, trunk and limbs (Stein, 1992; Ventre-Dominey et al., 2003). Regions within the posterior parietal cortex (PPC) integrate these multisensory inputs

Body representations

Ongoing bodily experience is fundamentally based on internal spatial representations of the body, which were first conceptualised by Münk and Bonnier in 1890 and 1905, respectively (Holmes and Spence, 2006; Maravita, 2006). Head and Holmes (1911–1912), however, made the first major advances in the development of concepts of body schemata. Bodily experience involves a complex integration of (a) automatic, bottom-up sensory and organisational processes (body schema) with (b) higher-order,

Body ownership and self-attribution

The sense of body ownership is defined as the perception that parts of the body phenomenologically and functionally belong to oneself (self-attribution). Body ownership thus stems from the convergence of multiple sensory inputs, particularly proprioceptive and visual inputs. Using the rubber limb paradigm (described below), Ehrsson et al. (2004) identified that the feeling of ownership of a seen limb was associated with premotor cortex activity, and that self-attribution may be related to

Embodiment

Embodiment involves the perception that one's sense of self is localised within one's bodily borders (Arzy et al., 2006c). Embodiment is not confined to the bodily self and may extend, for example, to a habitually used tool or prosthesis that effectively extend the body's area of influence. Embodiment is a complex process that involves representations of the self and the body, multi-sensory integration and motor intention and function. Arzy et al. (2006c) identified that the EBA and TPJ were

Illusory manipulations of self-attribution and embodiment

Body awareness, ownership and perception are modifiable aspects of conscious and unconscious experience. The plasticity of body perception has become apparent through research on visual capture, as well as through evidence of the internalisation of deployed tools, and the convergence between a phantom limb and a prosthesis or an intact limb and a rubber limb. These illusions of embodiment and bodily perception will now be described.

Conclusions

Bodily experience depends upon the integration of multi-sensory information relating to the body in space. Essentially, there are three aspects to bodily experience: (a) internal representations of the body; and the identification with parts of the body that are (b) attributed to the self and “owned”, and (c) embodied by oneself. Body ownership is enhanced through the mechanisms of visual capture that combine proprioceptive and visual information about limb position. Furthermore, predictive,

Acknowledgement

We would like to acknowledge the feedback provided by two anonymous reviewers.

References (205)

  • P. Giraux et al.

    Illusory movements of the paralyzed limb restore motor cortex activity

    Neuroimage

    (2003)
  • M.J. Giummarra et al.

    Central mechanisms in phantom limb perception: the past, present and future

    Brain Research Reviews

    (2007)
  • G.M. Goodwin et al.

    The persistence of appreciable kinaesthesia after paralysing joint afferents but preserving muscle afferents

    Brain Research

    (1972)
  • Y. Gross et al.

    Body image: dissociation of real and perceived limbs by pressure-cuff ischemia

    Experimental Neurology

    (1978)
  • Y. Gross et al.

    Central and peripheral contributions to localisation of body parts: evidence for a central body schema

    Experimental Neurology

    (1974)
  • P.W. Halligan et al.

    Unilateral somatoparaphrenia after right hemisphere stroke: a case description

    Cortex

    (1995)
  • A. Hill

    Phantom limb pain: a review of the literature on attributes and potential mechanisms

    Journal of Pain and Symptom Management

    (1999)
  • A. Hill et al.

    Pain memories in phantom limbs: a case study

    Pain

    (1996)
  • P.L. Jackson et al.

    How do we perceive the pain of others? A window into the neural processes involved in empathy

    NeuroImage

    (2005)
  • K. Ackroyd et al.

    Widening the sphere of influence: using a tool to extend extrapersonal space in a patient with severe neglect

    Neurocase

    (2002)
  • S. Aglioti et al.

    Disownership of left hand and objects related to it in a patient with right brain damage

    NeuroReport

    (1996)
  • S.H. Ambrose

    Paleolithic technology and human evolution

    Science

    (2001)
  • R.A. Andersen et al.

    Multimodal representation of space in the posterior parietal cortex and its use in planning movements

    Annual Review of Neuroscience

    (1997)
  • J.-M. André et al.

    L’illusion de normalité corporelle chez l’amputé et le paraplégique. Effets de la stimulation calorique vestibulaire sur les perceptions corporelles [Illusion of body normality in patients with limb amputation or total section of the spinal cord. Caloric vestibular stimulation effects on body representations]

    Revue Neurologique

    (2001)
  • J.M. André et al.

    Temporary phantom limbs evoked by vestibular caloric stimulation in amputees

    Neuropsychiatry, Neuropsychology, and Behavioural Neurology

    (2001)
  • K.C. Armel et al.

    Projecting sensations to external objects: evidence from skin conductance response

    Proceedings of the Royal Society of London Series B—Biological Sciences

    (2003)
  • S. Arzy et al.

    Neural mechanisms of embodiment: asomatognosia due to premotor cortex damage

    Archives of Neurology

    (2006)
  • S. Arzy et al.

    Induction of an illusory shadow person

    Nature

    (2006)
  • S. Arzy et al.

    Neural basis of embodiment: distinct contributions of temporoparietal junction and extrastriate body area

    The Journal of Neuroscience

    (2006)
  • F. Assal et al.

    Functional correlates of an alien hand syndrome: more insight in unconscious motor acts

    European Journal of Neurology

    (2006)
  • S.V. Astafiev et al.

    Extrastriate body area in human occipital cortex responds to the performance of motor actions

    Nature neuroscience

    (2004)
  • E.L. Austen et al.

    Mislocalisations of touch to a fake hand

    Cognitive, Affective, and Behavioural Neuroscience

    (2004)
  • M. Avillac et al.

    Reference frames for representing visual and tactile locations in parietal cortex

    Nature neuroscience

    (2005)
  • P. Bartolomeo et al.

    The influence of limb crossing on left tactile extinction

    Journal of Neurology Neurosurgery and Psychiatry

    (2004)
  • N. Berberovic et al.

    Prismatic adaptation reduces bised temporal order judgements in spatial neglect

    NeuroReport

    (2004)
  • A. Berti et al.

    When far becomes near: remapping of space by tool use

    Journal of Cognitive Neuroscience

    (2000)
  • I. Biran et al.

    The alien hand syndrome: what makes the alien hand alien?

    Cognitive Neuropsychology

    (2006)
  • S.-J. Blakemore et al.

    Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia

    Brain

    (2005)
  • O. Blanke

    Out of body experiences and their neural basis

    British Medical Journal

    (2004)
  • O. Blanke et al.

    The out-of-body experience: disturbed self-processing at the temporo-parietal junction

    The Neuroscientist

    (2005)
  • O. Blanke et al.

    Stimulating illusory own-body perceptions

    Nature

    (2002)
  • Bonda, E., Petrides, M., Frey, S., Evans, A., 1995. Neural correlates of mental transformations of the body-in-space....
  • E. Bors

    Phantom limbs in patients with spinal cord injury

    Archives Neurology Psychiatry

    (1951)
  • G. Bottini et al.

    Feeling touches in someone else's hand

    NeuroReport

    (2002)
  • M. Botvinick

    Probing the neural basis of body ownership

    Science

    (2004)
  • M. Botvinick et al.

    Rubber hands ‘feel’ touch that eyes see

    Nature

    (1998)
  • J.L. Bradshaw

    Human Evolution: A Neuropsychological Perspective

    (1997)
  • M. Braun et al.

    Feet dorsal imaginary flexion in paraplegic patients: fMRI of motor areas before and through vestibular stimulation

    NeuroImage

    (2001)
  • T. Breuer et al.

    First observation of tool use in wild gorillas

    Public Library of Science Biology

    (2005)
  • P.R. Bromage et al.

    Phantom limbs and the body schema

    Canadian Anaesthetics Society Journal

    (1974)
  • Cited by (0)

    View full text