Bisecting Real and Fake Body Parts: Effects of Prism Adaptation After Right Brain Damage

The representation of body parts holds a special status in the brain, due to their prototypical shape and the contribution of multisensory (visual and somatosensory-proprioceptive) information. In a previous study (Sposito et al., 2010), we showed that patients with left unilateral spatial neglect exhibit a rightward bias in setting the midpoint of their left forearm, which becomes larger when bisecting a cylindrical object comparable in size. This body part advantage, found also in control participants, suggests partly different processes for computing the extent of body parts and objects. In this study we tested 16 right-brain-damaged patients, and 10 unimpaired participants, on a manual bisection task of their own (real) left forearm, or a size-matched fake forearm. We then explored the effects of adaptation to rightward displacing prism exposure, which brings about leftward aftereffects. We found that all participants showed prism adaptation (PA) and aftereffects, with right-brain-damaged patients exhibiting a reduction of the rightward bias for both real and fake forearm, with no overall differences between them. Second, correlation analyses highlighted the role of visual and proprioceptive information for the metrics of body parts. Third, single-patient analyses showed dissociations between real and fake forearm bisections, and the effects of PA, as well as a more frequent impairment with fake body parts. In sum, the rightward bias shown by right-brain-damaged patients in bisecting body parts is reduced by prism exposure, as other components of the neglect syndrome; discrete spatial representations for real and fake body parts, for which visual and proprioceptive codes play different roles, are likely to exist. Multisensory information seems to render self bodily segments more resistant to the disruption brought about by right-hemisphere injury.

[1]  F. Vignemont Body schema and body image—Pros and cons , 2010, Neuropsychologia.

[2]  L. Gauthier,et al.  The Bells Test: A quantitative and qualitative test for visual neglect. , 1989 .

[3]  M. Bozkurt,et al.  Functional anatomy. , 1980, Equine veterinary journal.

[4]  M. Jeannerod,et al.  The Directional Coding of Reaching Movements. A Visuomotor Conception of Spatial Neglect , 1987 .

[5]  R. Newport,et al.  Evidence for dissociable representations for body image and body schema from a patient with visual neglect , 2011, Neurocase.

[6]  A Maravita,et al.  From "body in the brain" to "body in space". Sensory and intentional components of body representation , 2006 .

[7]  M. Perenin,et al.  Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect , 1998, Nature.

[8]  D. Perani,et al.  Unilateral neglect: Personal and extra-personal , 1986, Neuropsychologia.

[9]  G Rizzolatti,et al.  The Space Around Us , 1997, Science.

[10]  A. Maravita,et al.  Personal and Extrapersonal Spatial Perception , 2009 .

[11]  G Vallar,et al.  Processing of illusion of length in spatial hemineglect: a study of line bisection , 2000, Neuropsychologia.

[12]  J. Bradshaw,et al.  Mechanisms underlying embodiment, disembodiment and loss of embodiment , 2008, Neuroscience & Biobehavioral Reviews.

[13]  Y. Rossetti,et al.  Ameliorating neglect with prism adaptation: visuo-manual and visuo-verbal measures , 2002, Neuropsychologia.

[14]  R. Mayeux,et al.  Hemispatial neglect , 1989, Neurology.

[15]  L. Swan,et al.  Unilateral spatial neglect. , 2001, Physical therapy.

[16]  Umberto Sabatini,et al.  Neural bases of personal and extrapersonal neglect in humans. , 2007, Brain : a journal of neurology.

[17]  G. Vallar,et al.  Productive and Optic Prism Exposureproductive and Defective Impairments in the Neglect Syndrome: Graphic Perseveration, Drawing Productions and Optic Prism Exposure , 2006, Cortex.

[18]  Jacob Cohen Measurement Educational and Psychological Educational and Psychological Measurement Eta-squared and Partial Eta-squared in Fixed Factor Anova Designs Educational and Psychological Measurement Additional Services and Information For , 2022 .

[19]  H. Branch Coslett,et al.  Evidence for a Disturbance of the Body Schema in Neglect , 1998, Brain and Cognition.

[20]  S. Aglioti,et al.  The body in the brain: neural bases of corporeal awareness , 1997, Trends in Neurosciences.

[21]  Alessandro Farnè,et al.  In search of biased egocentric reference frames in neglect , 1998, Neuropsychologia.

[22]  L. Pizzamiglio,et al.  Cognitive rehabilitation of the hemineglect disorder in chronic patients with unilateral right brain damage. , 1992, Journal of clinical and experimental neuropsychology.

[23]  S. Aglioti,et al.  The body in the brain revisited , 2009, Experimental Brain Research.

[24]  H. Karnath,et al.  Subjective body orientation in neglect and the interactive contribution of neck muscle proprioception and vestibular stimulation. , 1994, Brain : a journal of neurology.

[25]  K. Heilman,et al.  Neglect and Related Disorders , 1984, Seminars in neurology.

[26]  L. Diller,et al.  Hemi-inattention in rehabilitation: the evolution of a rational remediation program. , 1977, Advances in neurology.

[27]  Y. Rossetti,et al.  After-effects of visuo-manual adaptation to prisms on body posture in normal subjects , 2002, Experimental Brain Research.

[28]  P. Faglioni,et al.  Recognition of random shapes by patients with unilateral lesions as a function of complexity, association value and delay. , 1974, Cortex; a journal devoted to the study of the nervous system and behavior.

[29]  Y. Rossetti,et al.  Functional anatomy of the therapeutic effects of prism adaptation on left neglect , 2006, Neurology.

[30]  Jonathan D. Cohen,et al.  Rubber hands ‘feel’ touch that eyes see , 1998, Nature.

[31]  Yves Rossetti,et al.  Dissociated long lasting improvements of straight-ahead pointing and line bisection tasks in two hemineglect patients , 2002, Neuropsychologia.

[32]  P. Downing,et al.  The effect of viewpoint on body representation in the extrastriate body area , 2004, Neuroreport.

[33]  H. C. Dijkerman,et al.  Acute neglect rehabilitation using repetitive prism adaptation: a randomized placebo-controlled trial. , 2008, Restorative neurology and neuroscience.

[34]  Alison J. Wiggett,et al.  The role of the extrastriate body area in action perception , 2006, Social neuroscience.

[35]  Costanza Papagno,et al.  Unawareness of disease following lesions of the right hemisphere: Anosognosia for hemiplegia and anosognosia for hemianopia , 1986, Neuropsychologia.

[36]  G. Holmes,et al.  Sensory disturbances from cerebral lesions , 1911 .

[37]  Wolff-Michael Roth,et al.  Body in Space , 2010 .

[38]  C. Urgesi,et al.  The Neural Basis of Body Form and Body Action Agnosia , 2008, Neuron.

[39]  C. Gross,et al.  The representation of extrapersonal space: A possible role for bimodal, visual-tactile neurons , 1995 .

[40]  J. Driver,et al.  Prism adaptation aftereffects in stroke patients with spatial neglect: Pathological effects on subjective straight ahead but not visual open-loop pointing , 2008, Neuropsychologia.

[41]  Yves Rossetti,et al.  Neglect and prism adaptation: a new therapeutic tool for spatial cognition disorders. , 2006, Restorative neurology and neuroscience.

[42]  Cristina Burani,et al.  Neglect dyslexia: a review of the neuropsychological literature , 2010, Experimental Brain Research.

[43]  Edoardo Bisiach,et al.  Line bisection and cognitive plasticity of unilateral neglect of space , 1983, Brain and Cognition.

[44]  Ehud Zohary,et al.  Is That Near My Hand? Multisensory Representation of Peripersonal Space in Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[45]  Giuseppe Vallar,et al.  Deficits of position sense, unilateral neglect and optokinetic stimulation , 1993, Neuropsychologia.

[46]  A. Milner,et al.  Prism Adaptation Improves Chronic Visual and Haptic Neglect: A Single Case Study , 2002, Cortex.

[47]  G. Vallar,et al.  Pierre Bonnier’s (1905) cases of bodily ‘aschematie’ , 2013 .

[48]  K. Goedert,et al.  Prism adaptation differently affects motor-intentional and perceptual-attentional biases in healthy individuals , 2011, Neuropsychologia.

[49]  N. Kanwisher,et al.  The Human Body , 2001 .

[50]  Nadia Bolognini,et al.  Proprioceptive Alignment of Visual and Somatosensory Maps in the Posterior Parietal Cortex , 2007, Current Biology.

[51]  F. Meneghello,et al.  Long-lasting amelioration of visuospatial neglect by prism adaptation. , 2002, Brain : a journal of neurology.

[52]  Nadia Bolognini,et al.  The spatial encoding of body parts in patients with neglect and neurologically unimpaired participants , 2010, Neuropsychologia.

[53]  Ronald Melzack,et al.  Body image: Dissociation of real and perceived limbs by pressure-cuff ischemia , 1978, Experimental Neurology.

[54]  Paul H Garthwaite,et al.  Testing for suspected impairments and dissociations in single-case studies in neuropsychology: evaluation of alternatives using monte carlo simulations and revised tests for dissociations. , 2005, Neuropsychology.

[55]  H. Karnath,et al.  Tight Link Between Our Sense of Limb Ownership and Self-Awareness of Actions , 2008, Stroke.

[56]  J. Marshall,et al.  Focal and global attention modulate the expression of visuo-spatial neglect: A case study , 1994, Neuropsychologia.

[57]  Personal and extra-personal spatial perception , 2009 .

[58]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[59]  R Tissot,et al.  Qualitative analysis of unilateral spatial neglect in relation to laterality of cerebral lesions , 1972, Journal of neurology, neurosurgery, and psychiatry.

[60]  C. Guariglia,et al.  Personal and extrapersonal space: A case of neglect dissociation , 1992, Neuropsychologia.

[61]  H. Karnath,et al.  Spatial orientation and the representation of space with parietal lobe lesions. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[62]  A. Sirigu,et al.  Multiple representations contribute to body knowledge processing. Evidence from a case of autotopagnosia. , 1991, Brain : a journal of neurology.

[63]  T. Schenkenberg,et al.  Line bisection and unilateral visual neglect in patients with neurologic impairment , 1980, Neurology.

[64]  Y. Rossetti,et al.  Effect of prism adaptation on left dichotic listening deficit in neglect patients: glasses to hear better? , 2010, Brain : a journal of neurology.

[65]  F. Doricchi,et al.  Misrepresentation of horizontal space in left unilateral neglect , 1999, Neurology.

[66]  S. Gallagher How the body shapes the mind , 2005 .

[67]  Nadia Bolognini,et al.  Review Article , 2003 .

[68]  Eleanor M. Saffran,et al.  Knowledge of the human body: A distinct semantic domain , 2002, Neurology.

[69]  A. Maravita,et al.  Rehabilitating patients with left spatial neglect by prism exposure during a visuomotor activity. , 2010, Neuropsychology.

[70]  Georg Kerkhoff,et al.  Spatial hemineglect in humans , 2001, Progress in Neurobiology.

[71]  Valeria I. Petkova,et al.  From Part- to Whole-Body Ownership in the Multisensory Brain , 2011, Current Biology.

[72]  P. Vuilleumier [Unilateral spatial neglect]. , 2003, Revue medicale de la Suisse romande.

[73]  C. Spence,et al.  Multisensory integration and the body schema: close to hand and within reach , 2003, Current Biology.

[74]  Hans-Otto Karnath,et al.  Awareness of the Functioning of One's Own Limbs Mediated by the Insular Cortex? , 2005, The Journal of Neuroscience.

[75]  Sylvie Chokron,et al.  Patterns of dissociation between left hemineglect and deviation of the egocentric reference , 1997, Neuropsychologia.

[76]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[77]  Jason B Mattingley,et al.  Effects of prismatic adaptation on judgements of spatial extent in peripersonal and extrapersonal space , 2003, Neuropsychologia.

[78]  Y. Rossetti,et al.  Cognitive bias induced by visuo‐motor adaptation to prisms: a simulation of unilateral neglect in normal individuals? , 2000, Neuroreport.

[79]  C. Gross,et al.  A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields , 1993, Experimental Brain Research.

[80]  G. Vallar,et al.  Somatoparaphrenia: a body delusion. A review of the neuropsychological literature , 2008, Experimental Brain Research.

[81]  Giuseppe Vallar,et al.  Exploring the syndrome of spatial unilateral neglect through an illusion of length , 2002, Experimental Brain Research.

[82]  S. Chokron Right parietal lesions, unilateral spatial neglect, and the egocentric frame of reference , 2003, NeuroImage.

[83]  G. Vallar,et al.  Visuo-Haptic Interactions in Unilateral Spatial Neglect: The Cross Modal Judd Illusion , 2011, Front. Psychology.

[84]  M. Perenin,et al.  Temporary remission of representational hemineglect through vestibular stimulation. , 1994, Neuroreport.

[85]  Gordon M. Redding,et al.  Applications of prism adaptation: a tutorial in theory and method , 2005, Neuroscience & Biobehavioral Reviews.

[86]  J. Cole,et al.  Body image and body schema in a deafferented subject , 1995 .

[87]  D. Boisson,et al.  Does Action Make the Link Between Number and Space Representation? , 2004, Psychological science.

[88]  Y. Rossetti,et al.  Left size distortion (hyperschematia) after right brain damage , 2006, Neurology.

[89]  C. Gross,et al.  Coding of visual space by premotor neurons. , 1994, Science.

[90]  H. Karnath,et al.  The anatomy of spatial neglect , 2012, Neuropsychologia.

[91]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[92]  A. Maravita,et al.  Prism adaptation can improve contralesional tactile perception in neglect , 2003, Neurology.

[93]  M. Husain Hemispatial neglect. , 2008, Handbook of clinical neurology.

[94]  R. Passingham,et al.  That's My Hand! Activity in Premotor Cortex Reflects Feeling of Ownership of a Limb , 2004, Science.