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

Phantom limbs provide valuable insight into the mechanisms underlying bodily awareness and ownership. This paper reviews the complexity of phantom limb phenomena (proprioception, form, position, posture and telescoping), and the various contributions of internal constructs of the body, or body schema, and neuromatrix theory in explaining these phenomena. Specific systems and processes that have received little attention in phantom limb research are also reviewed and highlighted as important future directions, These include prosthesis embodiment and extended physiological proprioception (i.e., the extension of the body's "area of influence" that thereby extends one's innate sense of proprioception, mirror neurons and cross-referencing of the phantom limb with the intact limb (and the related phenomena of perceiving referred sensations and mirrored movements in the phantom form the intact limb). The likely involvements of the body schema and the body-self neuromatrix, mirror neurons, and cross-callosal and ipsilateral mechanisms in phantom limb phenomena all suggest that the perception of a "normal" phantom limb (that is, a non-painful phantom that has the sensory qualities of an intact limb) is more than likely an epiphenomenon of normal functioning, action understanding and empathy, and potentially may even be evolutionarily adaptive and perhaps necessary. Phantom pain, however, may be a maladaptive failure of the neuromatrix to maintain global bodily constructs.

[1]  H. Flor,et al.  Phantom limb pain: a case of maladaptive CNS plasticity? , 2006, Nature Reviews Neuroscience.

[2]  J Valls-Solé,et al.  Rapid modulation of human cortical motor outputs following ischaemic nerve block. , 1993, Brain : a journal of neurology.

[3]  Vittorio Gallese,et al.  Mirror Neurons and the Evolution of Brain and Language , 2002 .

[4]  J. Donoghue,et al.  Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[6]  Shaun Gallagher,et al.  Body image and body schema: A conceptual clarification. , 1986 .

[7]  P. Ovesen,et al.  Phantom-related phenomena after rectal amputation: prevalence and clinical characteristics , 1991, Pain.

[8]  R. Kaplan Treatment of homosexuality during apartheid , 2004, BMJ : British Medical Journal.

[9]  S. Tipper,et al.  Implicit action encoding influences personal-trait judgments , 2007, Cognition.

[10]  K. Jamison,et al.  Phantom breast syndrome. , 1979, Archives of surgery.

[11]  J. Mattingley,et al.  Allodynia: a sensory analogue of motor mirror neurons in a hyperaesthetic patient reporting instantaneous discomfort to another's perceived sudden minor injury? , 2001, Journal of neurology, neurosurgery, and psychiatry.

[12]  On embodiment: A case study of congenital limb deficiency in American culture , 1986, Culture, medicine and psychiatry.

[13]  Martin Tegenthoff,et al.  Reorganization in the ipsilateral motor cortex of patients with lower limb amputation , 2003, Neuroscience Letters.

[14]  J. Marshall,et al.  Sensory disorganization and perceptual plasticity after limb amputation: a follow‐up study , 1994, Neuroreport.

[15]  S. Weinstein,et al.  Phantoms in cases of congenital absence of limbs , 1961, Neurology.

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

[17]  R M Müri,et al.  Beyond re-membering: phantom sensations of congenitally absent limbs. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[19]  P. McGrath,et al.  Prospective Diary Study of Nonpainful and Painful Phantom Sensations in a Preselected Sample of Child and Adolescent Amputees Reporting Phantom Limbs , 2004, The Clinical journal of pain.

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

[21]  J. Marshall,et al.  Unilateral Somatoparaphrenia After Right Hemisphere Stroke: A Case Description , 1995, Cortex.

[22]  S. Brena,et al.  Phantom urinary bladder pain — case report , 1979, Pain.

[23]  M. Tanaka,et al.  Coding of modified body schema during tool use by macaque postcentral neurones. , 1996, Neuroreport.

[24]  C. Fraser Fact and Fiction: A Clarification of Phantom Limb Phenomena , 2002 .

[25]  M. Shiffrar,et al.  Hand movement observation by individuals born without hands: phantom limb experience constrains visual limb perception , 2005, Experimental Brain Research.

[26]  S. Evers,et al.  Phantom eye syndrome , 2003, Neurology.

[27]  L. Cohen,et al.  Modulation of Plasticity in Human Motor Cortex after Forearm Ischemic Nerve Block , 1998, The Journal of Neuroscience.

[28]  Fisher Cm Phantom erection after amputation of penis. Case description and review of the relevant literature on phantoms. , 1999 .

[29]  E. Bors Phantom limbs of patients with spinal cord injury. , 1951, A.M.A. archives of neurology and psychiatry.

[30]  H. Flor,et al.  Effect of sensory discrimination training on cortical reorganisation and phantom limb pain , 2001, The Lancet.

[31]  S. Ho,et al.  Prevalence and clinical characteristics of phantom rectum syndrome after rectum resection in Chinese patients , 2001 .

[32]  F. Sartucci,et al.  Supernumerary phantom limb after ischaemic stroke , 1997 .

[33]  N. Schiff,et al.  Does vestibular stimulation activate thalamocortical mechanisms that reintegrate impaired cortical regions? , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  V. Gallese The ‘‘shared manifold’’ hypothesis: from mirror neurons to empathy , 2001 .

[35]  T Steinbach,et al.  Phantom limbs and related phenomena in recent traumatic amputations , 1978, Neurology.

[36]  T. Ettlin,et al.  Phantom and amputation illusions in paraplegic patients. , 1980, European neurology.

[37]  G. Butterworth,et al.  Hand–Mouth Coordination, Congenital Absence of Limb, and Evidence for Innate Body Schemas , 1998, Brain and Cognition.

[38]  H. Branch Coslett,et al.  Evidence for Multiple, Distinct Representations of the Human Body , 2005, Journal of Cognitive Neuroscience.

[39]  S. Aglioti,et al.  Disownership of left hand and objects related to it in a patient with right brain damage , 1996, Neuroreport.

[40]  N Nighoghossian,et al.  Evidence for interacting cortical control of vestibular function and spatial representation in man , 2003, Neuropsychologia.

[41]  Elfed Huw Price A critical review of congenital phantom limb cases and a developmental theory for the basis of body image , 2006, Consciousness and Cognition.

[42]  P. Halligan,et al.  Hypnotic imagery as a treatment for phantom limb pain: two case reports and a review , 2002, Clinical rehabilitation.

[43]  K. Poeck,et al.  Phantoms Following Amputation in Early Childhood and in Congenital Absence of Limbs , 1964 .

[44]  R Melzack,et al.  Phantom limbs in people with congenital limb deficiency or amputation in early childhood. , 1997, Brain : a journal of neurology.

[45]  John L. Bradshaw,et al.  Investigating the cortical origins of motor overflow , 2004, Brain Research Reviews.

[46]  Neil Levy,et al.  Amputees by choice: body integrity identity disorder and the ethics of amputation. , 2005, Journal of applied philosophy.

[47]  P. Halligan,et al.  Somesthetic aura: the experience of “Alice in Wonderland” , 1998, The Lancet.

[48]  Luciano Fadiga,et al.  The mirror system in humans , 2002 .

[49]  N Birbaumer,et al.  Phantom limb pain: cortical plasticity and novel therapeutic approaches , 2000, Current opinion in anaesthesiology.

[50]  C. Murray,et al.  Body image and prosthesis satisfaction in the lower limb amputee , 2002, Disability and rehabilitation.

[51]  J R Lackner,et al.  Reciprocal interactions between the position sense representations of the two forearms , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  C. Murray,et al.  An interpretative phenomenological analysis of the embodiment of artificial limbs , 2004, Disability and rehabilitation.

[53]  A. C. de C. Williams,et al.  Stiff upper lip: coping strategies of World War II veterans with phantom limb pain. , 1998, The Clinical journal of pain.

[54]  E. Brodie,et al.  Increased motor control of a phantom leg in humans results from the visual feedback of a virtual leg , 2003, Neuroscience Letters.

[55]  Malcolm MacLachlan,et al.  Mirror treatment of lower limb phantom pain: A case study , 2004, Disability and rehabilitation.

[56]  O. Blanke,et al.  The Out-of-Body Experience: Disturbed Self-Processing at the Temporo-Parietal Junction , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[57]  Malcolm MacLachlan,et al.  Enabling technologies : body image and body function , 2004 .

[58]  J. Marbach Is phantom tooth pain a deafferentation (neuropathic) syndrome? Part I: Evidence derived from pathophysiology and treatment. , 1993, Oral surgery, oral medicine, and oral pathology.

[59]  K. Sathian,et al.  Intermanual referral of sensation to anesthetic hands , 2000, Neurology.

[60]  R. Melzack,et al.  Pain ‘memories’ in phantom limbs: review and clinical observations , 1990, Pain.

[61]  L. Jones Motor Illusions: What Do They Reveal About Proprioception? , 1988 .

[62]  H. Flor,et al.  Phantom-limb pain: characteristics, causes, and treatment , 2002, The Lancet Neurology.

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

[64]  N. Miyazawa,et al.  Supernumerary Phantom Limbs Associated with Left Hemispheric Stroke: Case Report and Review of the Literature , 2004, Neurosurgery.

[65]  F. Binkofski,et al.  The mirror neuron system and action recognition , 2004, Brain and Language.

[66]  H. Flor,et al.  Phantom movements and pain. An fMRI study in upper limb amputees. , 2001, Brain : a journal of neurology.

[67]  V. Ramachandran,et al.  The perception of phantom limbs. The D. O. Hebb lecture. , 1998, Brain : a journal of neurology.

[68]  G. Pellegrino,et al.  Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue? , 2004, Cognitive, affective & behavioral neuroscience.

[69]  S. Kitazawa,et al.  Referral of tactile sensation to the tips of L-shaped sticks. , 2005, Journal of neurophysiology.

[70]  J. Paysant,et al.  Vestibular caloric stimulation evokes phantom limb illusions in patients with paraplegia , 2001, Spinal Cord.

[71]  S. Weinstein,et al.  Phantoms and Somatic Sensation in Cases of Congenital Aplasia , 1964 .

[72]  P. Wall,et al.  A controlled pilot study of the utility of mirror visual feedback in the treatment of complex regional pain syndrome (type 1). , 2003, Rheumatology.

[73]  S. Weinstein Phantom limb pain and related disorders. , 1998, Neurologic clinics.

[74]  J. Donoghue,et al.  Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions , 2004, Experimental Brain Research.

[75]  D. Price PHANTOM LIMB PHENOMENON IN PATIENTS WITH LEPROSY , 1976, The Journal of nervous and mental disease.

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

[77]  G. Moseley,et al.  Dysynchiria: Watching the mirror image of the unaffected limb elicits pain on the affected side , 2005, Neurology.

[78]  T Landis,et al.  Illusory Reduplication of One's Own Body: Phenomenology and Classification of Autoscopic Phenomena. , 1997, Cognitive neuropsychiatry.

[79]  O. Blanke Out of body experiences and their neural basis , 2004, BMJ : British Medical Journal.

[80]  Malcolm MacLachlan,et al.  Reaching with electricity: externally powered prosthetics and embodiment , 2004 .

[81]  K. Solonen The phantom phenomenon in amputated Finnish war veterans. , 1962, Acta orthopaedica Scandinavica. Supplementum.

[82]  R. Melzack Pain and the neuromatrix in the brain. , 2001, Journal of dental education.

[83]  V. Ramachandran,et al.  Synaesthesia in phantom limbs induced with mirrors , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[84]  JamesW. Lewis Cortical Networks Related to Human Use of Tools , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[85]  T. Murai,et al.  A third arm on the chest: implications for the cortical reorganization theory of phantom limbs. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[86]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

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

[88]  R. Melzack,et al.  Experimental phantom limbs. , 1973, Experimental neurology.

[89]  W. McIlroy,et al.  Adaptation in the motor cortex following cervical spinal cord injury , 2002, Neurology.

[90]  P. Mcdonnell,et al.  Do artificial limbs become part of the user? New evidence. , 1989, Journal of rehabilitation research and development.

[91]  B Craske,et al.  Perception of impossible limb positions induced by tendon vibration. , 1977, Science.

[92]  Ronald Melzack,et al.  Phantom limbs and the body schema , 1974 .

[93]  V. Ramachandran,et al.  Projecting sensations to external objects: evidence from skin conductance response , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[94]  S. Fishman,et al.  Extended and telescoped phantom limbs in unilateral amputees. , 1963 .

[95]  F. Cortese,et al.  Rapid sensory remapping in the adult human brain as inferred from phantom breast perception. , 1994, Neuroreport.

[96]  V. Ramachandran,et al.  Touching the phantom limb , 1995, Nature.

[97]  G. Miller Reflecting on Another's Mind , 2005, Science.

[98]  W. Everaerd,et al.  The relationship between involuntary pelvic floor muscle activity, muscle awareness and experienced threat in women with and without vaginismus. , 2001, Behaviour research and therapy.

[99]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[100]  E. Laan,et al.  Modulation of spinal reflexes by aversive and sexually appetitive stimuli. , 2003, Psychophysiology.

[101]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[102]  L. Craighero,et al.  Human motor cortex excitability during the perception of others’ action , 2005, Current Opinion in Neurobiology.

[103]  Gaspare Galati,et al.  Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain , 2005, Nature Neuroscience.

[104]  T. Aziz,et al.  Deep brain stimulation for phantom limb pain , 2005, Journal of Clinical Neuroscience.

[105]  P. Brugger Supernumerary Phantoms: A Comment on Grossi, et al.'s (2002) Spare Thoughts on Spare Limbs , 2003, Perceptual and motor skills.

[106]  V. Ramachandran,et al.  Encyclopedia of the Human Brain , 2002 .

[107]  Riitta Hari,et al.  Three hands: fragmentation of human bodily awareness , 1998, Neuroscience Letters.

[108]  Ronald Melzack,et al.  From the gate to the neuromatrix , 1999, Pain.

[109]  A. J. Harris,et al.  Cortical origin of pathological pain , 1999, The Lancet.

[110]  N. Birbaumer,et al.  Does use of a myoelectric prosthesis prevent cortical reorganization and phantom limb pain? , 1999, Nature Neuroscience.

[111]  Michael B First,et al.  Desire for amputation of a limb: paraphilia, psychosis, or a new type of identity disorder , 2004, Psychological Medicine.

[112]  C I Moore,et al.  Referred phantom sensations and cortical reorganization after spinal cord injury in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[113]  D. Gupta,et al.  Phantom Limb: A Phenomenological Study , 1982, British Journal of Psychiatry.

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

[115]  Elizabeth Corcoran,et al.  The MBAs of Summer , 1992 .

[116]  J. Stein The representation of egocentric space in the posterior parietal cortex. , 1992, The Behavioral and brain sciences.

[117]  V. Cruz,et al.  Cortical remapping in amputees and dysmelic patients: a functional MRI study. , 2003, NeuroRehabilitation.

[118]  J. André,et al.  Feet dorsal imaginary flexion in paraplegic patients : fMRI of motor areas before and through vestibular stimulation , 2001, NeuroImage.

[119]  G. Riddoch PHANTOM LIMBS AND BODY SHAPE1 , 1941 .

[120]  J. Bradshaw,et al.  The effects of age and attention on motor overflow production—A review , 2007, Brain Research Reviews.

[121]  J C Rothwell,et al.  Reorganization of cortical blood flow and transcranial magnetic stimulation maps in human subjects after upper limb amputation. , 1994, Journal of neurophysiology.

[122]  C. Frith,et al.  Whose arm is it anyway? An fMRI case study of supernumerary phantom limb. , 2002, Brain : a journal of neurology.

[123]  Karen D Davis,et al.  The effect of tactile and visual sensory inputs on phantom limb awareness. , 2003, Brain : a journal of neurology.

[124]  C. Spence,et al.  Beyond the body schema: Visual, prosthetic, and technological contributions to bodily perception and awareness , 2006 .

[125]  Stefano Facchini,et al.  Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements , 2005, NeuroImage.

[126]  J. Summers,et al.  Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability , 2005, Experimental Brain Research.

[127]  M. Shiffrar,et al.  Human Body Perception From The Inside Out , 2005 .

[128]  J. Arcadi "Phantom bladder": is this an unusual entity? , 1977, The Journal of urology.

[129]  S. I. Cohen,et al.  BILATERAL BREAST PHANTOM AND BREAST PHANTOM PAIN: Case Report , 1955, The Journal of nervous and mental disease.

[130]  R. Melzack,et al.  Phantom Limb Experiences in Congenital Limb-Deficient Adults , 1994, Cortex.

[131]  R. Melzack Phantom limbs, the self and the brain (the D. O. Hebb Memorial Lecture). , 1989 .

[132]  John Schwoebel,et al.  The man who executed “imagined” movements: Evidence for dissociable components of the body schema , 2002, Brain and Cognition.

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

[134]  C. Armatas,et al.  The Influence of Task Characteristics on the Intermanual Asymmetry of Motor Overflow , 2001, Journal of clinical and experimental neuropsychology.

[135]  Abi Berger,et al.  Phantoms in the brain , 1999, BMJ.

[136]  P. Halligan,et al.  Joint stiffness in a phantom limb: evidence of central nervous system involvement in rheumatoid arthritis. , 2003, Rheumatology.

[137]  I Berry,et al.  Virtual Movements Activate Primary Sensorimotor Areas in Amputees: Report of Three Cases , 2001, Neurosurgery.

[138]  A Hill,et al.  Phantom limb pain: a review of the literature on attributes and potential mechanisms. , 1999, Journal of pain and symptom management.

[139]  S. Kitazawa,et al.  Sensation at the tips of invisible tools , 2001, Nature Neuroscience.

[140]  P. Dijkstra,et al.  Phantom pain and phantom sensations in upper limb amputees: an epidemiological study , 2000, Pain.

[141]  G. Rizzolatti,et al.  Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. , 2005, Brain research. Cognitive brain research.

[142]  H. Helmholtz,et al.  Science and Culture: Popular and Philosophical Essays , 1995 .

[143]  F. Biley Phantom bladder sensations: a new concern for stoma care workers. , 2001, British journal of nursing.

[144]  J. B. Green,et al.  An electromyographic study of mirror movements , 1967, Neurology.

[145]  V. S. Ramachandran,et al.  Bimanual coupling in amputees with phantom limbs , 1998, Nature Neuroscience.

[146]  Henrik Walter,et al.  Neural correlates of frustration , 2005, Neuroreport.

[147]  R. Melzack Gate control theory , 1996 .

[148]  J. Lackner Some proprioceptive influences on the perceptual representation of body shape and orientation. , 1988, Brain : a journal of neurology.

[149]  L. Fogassi,et al.  A Touching Sight SII/PV Activation during the Observation and Experience of Touch , 2004, Neuron.

[150]  Maureen Dennis,et al.  Impaired sensory and motor differentiation with corpus callosum agenesis: A lack of callosal inhibition during ontogeny? , 1976, Neuropsychologia.

[151]  S-J Blakemore,et al.  Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. , 2005, Brain : a journal of neurology.

[152]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[153]  O. Blanke,et al.  Neural mechanisms of embodiment: asomatognosia due to premotor cortex damage. , 2006, Archives of neurology.

[154]  V. Moro,et al.  Illusory movements of the contralesional hand in patients with body image disorders , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[155]  I. Smith,et al.  Phantom rectum after complete rectal excision , 1968, The British journal of surgery.

[156]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

[157]  K. Reilly,et al.  Mapping phantom movement representations in the motor cortex of amputees. , 2006, Brain : a journal of neurology.

[158]  J. Conomy,et al.  Disorders of body image after spinal cord injury , 1973, Neurology.

[159]  Joel Katz,et al.  Psychophysiological Contributions to Phantom Limbs * , 1992, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[160]  R. Carson Neural pathways mediating bilateral interactions between the upper limbs , 2005, Brain Research Reviews.

[161]  J. Paysant,et al.  Temporary phantom limbs evoked by vestibular caloric stimulation in amputees. , 2001, Neuropsychiatry, neuropsychology, and behavioral neurology.

[162]  S. Kiebel,et al.  Structural and functional cortical abnormalities after upper limb amputation during childhood , 2001, Neuroreport.

[163]  M Schwaiger,et al.  Phantom limb pain in the human brain: Unraveling neural circuitries of phantom limb sensations using positron emission tomography , 2000, Annals of neurology.