The perception of phantom limbs. The D. O. Hebb lecture.

Almost everyone who has a limb amputated will experience a phantom limb--the vivid impression that the limb is not only still present, but in some cases, painful. There is now a wealth of empirical evidence demonstrating changes in cortical topography in primates following deafferentation or amputation, and this review will attempt to relate these in a systematic way to the clinical phenomenology of phantom limbs. With the advent of non-invasive imaging techniques such as MEG (magnetoencephalogram) and functional MRI, topographical reorganization can also be demonstrated in humans, so that it is now possible to track perceptual changes and changes in cortical topography in individual patients. We suggest, therefore, that these patients provide a valuable opportunity not only for exploring neural plasticity in the adult human brain but also for understanding the relationship between the activity of sensory neurons and conscious experience. We conclude with a theory of phantom limbs, some striking demonstrations of phantoms induced in normal subjects, and some remarks about the relevance of these phenomena to the question of how the brain constructs a 'body image.'

[1]  S. Weir Mitchell,et al.  Injuries to Nerves and Their Consequences , 1872, Buffalo Medical and Surgical Journal.

[2]  F. W. Mott,et al.  Experiments on the Influence of Sensory Nerves upon Movement and Nutrition of the Limbs. , 1895 .

[3]  T. Brown,et al.  On the Instability of a Cortical Point , 1912 .

[4]  H. Head SENSATION AND THE CEREBRAL CORTEX , 1918 .

[5]  E. Adrian,et al.  The impulses produced by sensory nerve‐endings , 1926 .

[6]  P. Schilder The Image and Appearance of the Human Body: Studies in the Constructive Energies of the Psyche , 1936 .

[7]  W. R. Brain VISUAL DISORIENTATION WITH SPECIAL REFERENCE TO LESIONS OF THE RIGHT CEREBRAL HEMISPHERE , 1941 .

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

[9]  K. Livingston The Phantom Limb Syndrome. A Discussion of the Role of Major Peripheral Nerve Neuromas , 1945 .

[10]  J. Gallagher,et al.  DORSAL CORDOTOMY FOR PAINFUL PHANTOM LIMB , 1948, Annals of surgery.

[11]  T. Szasz Psychiatric aspects of vagotomy; phantom ulcer pain. , 1949, Archives of neurology and psychiatry.

[12]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[13]  B. Cronholm Phantom limbs in amputees; a study of changes in the integration of centripetal impulses with special reference to referred sensations. , 1951, Acta psychiatrica et neurologica Scandinavica. Supplementum.

[14]  Phantom limb of forearm stump cleft by kineplastic surgery. , 1952, Journal international de chirurgie.

[15]  Kallio Ke Phantom limb of forearm stump cleft by kineplastic surgery. , 1952 .

[16]  FACIAL PHANTOM PHENOMENON , 1955, The Journal of nervous and mental disease.

[17]  THE PHANTOM LIMB: A PROPOSED THEORY OF UNCONSCIOUS ORIGINS , 1956, The Journal of nervous and mental disease.

[18]  M. Simmel Phantoms in patients with leprosy and in elderly digital amputees. , 1956, American Journal of Psychology.

[19]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[20]  J. Diamond,et al.  The effects of injecting acetylcholine into normal and regenerating nerves , 1959, The Journal of physiology.

[21]  J. Talairach,et al.  [Parietal surgery of pain]. , 1960, Acta neurochirurgica.

[22]  S. Landgren Thalamic neurones responding to cooling of the cat's tongue. , 1960, Acta physiologica Scandinavica.

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

[24]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

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

[26]  Sensory responses to subcortical stimulation and management of pain disorders by stereotaxic methods. , 1966, Confinia neurologica.

[27]  M. Critchley The parietal lobes , 1966 .

[28]  O. Appenzeller,et al.  Effects of nervous system lesions on phantom experience in amputees , 1969, Neurology.

[29]  P K Thomas,et al.  Composition of Peripheral Nerves , 1969 .

[30]  K. Poeck,et al.  Phantome nach Amputation und bei angeborenem Gliedmaßenmangel , 1969 .

[31]  K Poeck [Phantom limbs after amputation and in congenital missing limbs]. , 1969, Deutsche medizinische Wochenschrift.

[32]  P K Thomas,et al.  Nerves and Nerve Injuries , 1969 .

[33]  J. Kaas,et al.  Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[34]  I. Zimmerman,et al.  Cortical unit responses to temperature stimulation of the skin. , 1971, Brain research.

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

[36]  C. Parkes Factors determining the persistence of phantom pain in the amputee. , 1973, Journal of psychosomatic research.

[37]  Patrick D. Wall,et al.  Properties of afferent nerve impulses originating from a neuroma , 1974, Nature.

[38]  P. Wall The presence of ineffective synapses and the circumstances which unmask them. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[40]  D H Hubel,et al.  Brain mechanisms of vision. , 1979, Scientific American.

[41]  J. Kaas,et al.  The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex , 1979, The Journal of comparative neurology.

[42]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[43]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[44]  S. Zeki The representation of colours in the cerebral cortex , 1980, Nature.

[45]  Daniel C. Dennett,et al.  Brainstorms: Philosophical Essays on Mind and Psychology , 1981 .

[46]  David P. Friedman,et al.  Thalamic basis of place- and modality-specific columns in monkey somatosensory cortex: a correlative anatomical and physiological study. , 1982, Journal of neurophysiology.

[47]  C. Woolf Evidence for a central component of post-injury pain hypersensitivity , 1983, Nature.

[48]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[49]  T. Jensen,et al.  Phantom limb, phantom pain and stump pain in amputees during the first 6 months following limb amputation , 1983, Pain.

[50]  P. Wall The Painful Consequences of Peripheral Injury , 1984, Journal of hand surgery.

[51]  K. Reinikainen,et al.  A four-channel SQUID magnetometer for brain research. , 1984, Electroencephalography and clinical neurophysiology.

[52]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[53]  Richard A. Sherman,et al.  Chronic phantom and stump pain among american veterans: results of a survey , 1984, Pain.

[54]  T. Jensen,et al.  Immediate and long-term phantom limb pain in amputees: Incidence, clinical characteristics and relationship to pre-amputation limb pain , 1985, Pain.

[55]  Mriganka Sur,et al.  Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1 , 1985, Brain Research.

[56]  C. Sherrington,et al.  VIII. Experiments upon the influence of sensory nerves upon movement and nutrition of the limbs. Preliminary communication , 1985, Proceedings of the Royal Society of London.

[57]  E G Jones,et al.  Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  W. Roberts A hypothesis on the physiological basis for causalgia and related pains , 1986, Pain.

[59]  N. Postone Phantom Limb Pain. A Review , 1988, International journal of psychiatry in medicine.

[60]  Bereavement: Studies of Grief in Adult Life (2nd edition). By Colin Murray Parkes. London: Tavistock. 1986. Pp. 265. £12.00. , 1987, British Journal of Psychiatry.

[61]  L. Weiskrantz,et al.  Residual tactile sensitivity with self-directed stimulation in hemianaesthesia. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[62]  R. Meyer,et al.  Painful sequelae of nerve injury , 1987, PAIN.

[63]  L. Cooper,et al.  A physiological basis for a theory of synapse modification. , 1987, Science.

[64]  M. Mishkin,et al.  Lesion-induced plasticity in the second somatosensory cortex of adult macaques. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

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

[66]  R. Melzack,et al.  An association between phantom limb sensations and stump skin conductance during transcutaneous electrical nerve stimulation (TENS) applied to the contralateral leg: a case study , 1989, Pain.

[67]  B. Krebs,et al.  Immediate and long-term phantom breast syndrome after mastectomy: incidence, clinical characteristics and relationship to pre-mastectomy breast pain , 1989, Pain.

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

[69]  J. Bruer The Remembered Present: A Biological Theory of Consciousness , 1990 .

[70]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[71]  E. Jones,et al.  The role of afferent activity in the maintenance of primate neocorticalfunction. , 1990, The Journal of experimental biology.

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

[73]  S. Bandinelli,et al.  Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. , 1991, Brain : a journal of neurology.

[74]  M. Calford,et al.  Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation. , 1991, Somatosensory & motor research.

[75]  J. Kaas,et al.  Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining. , 1991, Somatosensory & motor research.

[76]  R. L. Gregory,et al.  Perceptual filling in of artificially induced scotomas in human vision , 1991, Nature.

[77]  M. Calford Curious cortical change , 1991, Nature.

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

[79]  D. Bosch Stereotactic rostral mesencephalotomy in cancer pain and deafferentation pain. A series of 40 cases with follow-up results. , 1991, Journal of neurosurgery.

[80]  Michael B. Calford,et al.  Short-term expansion of receptive fields in rat primary somatosensory cortex after hindpaw digit denervation , 1991, Brain Research.

[81]  M. Calford,et al.  C-fibres provide a source of masking inhibition to primary somatosensory cortex , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[82]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[83]  V. Ramachandran,et al.  Perceptual correlates of massive cortical reorganization. , 1992, Science.

[84]  J.C. Mosher,et al.  Multiple dipole modeling and localization from spatio-temporal MEG data , 1992, IEEE Transactions on Biomedical Engineering.

[85]  E. Taub,et al.  Chronic deafferentation in monkeys differentially affects nociceptive and nonnociceptive pathways distinguished by specific calcium-binding proteins and down-regulates gamma-aminobutyric acid type A receptors at thalamic levels. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[86]  R. Melzack,et al.  Multiple Phantom Limbs in a Child , 1992, Cortex.

[87]  V S Ramachandran,et al.  Blind Spots , 2011, The American journal of bioethics : AJOB.

[88]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[89]  M. Pettet,et al.  Dynamic changes in receptive-field size in cat primary visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[90]  R. Melzack Phantom Limbs , 1989, Regional Anesthesia & Pain Medicine.

[91]  S. Hahn Motor Reorganization After Upper Limb Amputation in Man , 1992 .

[92]  J. Marshall,et al.  Thumb in cheek? Sensory reorganization and perceptual plasticity after limb amputation. , 1993, Neuroreport.

[93]  N. Miller,et al.  Technique to improve chronic motor deficit after stroke. , 1993, Archives of physical medicine and rehabilitation.

[94]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[95]  F E Bloom,et al.  Noninvasive presurgical neuromagnetic mapping of somatosensory cortex. , 1993, Neurosurgery.

[96]  J. Marshall,et al.  Three arms: a case study of supernumerary phantom limb after right hemisphere stroke. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[97]  V. Ramachandran,et al.  Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[98]  V. S. Ramachandran Filling in Gaps in Logic: Some Comments on Dennett , 1993, Consciousness and Cognition.

[99]  Auditory perceptual and visual-spatial characteristics of gaze-evoked tinnitus. , 1994, Audiology : official organ of the International Society of Audiology.

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

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

[102]  F. E. Bloom,et al.  Sensory maps in the human brain , 1994, Nature.

[103]  V S Ramachandran,et al.  Noninvasive detection of cerebral plasticity in adult human somatosensory cortex. , 1994, Neuroreport.

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

[105]  S. Schug,et al.  Pre-emptive Epidural Analgesia May Prevent Phantom Limb Pain , 1994, Regional Anesthesia & Pain Medicine.

[106]  S. Aglioti,et al.  Phantom lower limb as a perceptual marker of neural plasticity in the mature human brain , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[107]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[108]  J. Kaas,et al.  Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  M. Sur,et al.  Activity-dependent remodeling of connections in the mammalian visual system , 1995, Current Opinion in Neurobiology.

[110]  R. Dykes,et al.  Evolution of cortical responsiveness subsequent to multiple forelimb nerve transections: An electrophysiological study in adult cat somatosensory cortex , 1995, The Journal of comparative neurology.

[111]  J. Marshall,et al.  Supernumerary phantom limb after right hemispheric stroke. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[112]  J. Liepert,et al.  Changes of cortical motor area size during immobilization. , 1995, Electroencephalography and clinical neurophysiology.

[113]  V. Ramachandran Anosognosia in Parietal Lobe Syndrome , 1995, Consciousness and Cognition.

[114]  Peter De Weerd,et al.  Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma , 1995, Nature.

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

[116]  T. Elbert,et al.  Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation , 1995, Nature.

[117]  Phantom face: conscious correlate of neural reorganization after removal of primary sensory neurones , 1996, Neuroreport.

[118]  Jon H. Kaas,et al.  Brain Reorganization and Experience , 1996 .

[119]  J. Flanagan,et al.  Hand and brain : the neurophysiology and psychology of hand movements , 1996 .

[120]  M Hallett,et al.  Transcranial magnetic stimulation: a tool for mapping the central nervous system. , 1996, Electroencephalography and clinical neurophysiology. Supplement.

[121]  Jon H. Kaas,et al.  Central reorganization of sensory pathways following peripheral nerve regeneration in fetal monkeys , 1996, Nature.

[122]  T Landis,et al.  Plasticity in the adult visual cortex: implications for the diagnosis of visual field defects and visual rehabilitation , 1996, Current opinion in ophthalmology.

[123]  Á. Pascual-Leone,et al.  Reorganization of human cortical motor output maps following traumatic forearm amputation , 1996, Neuroreport.

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

[125]  P. Churchland,et al.  The Mind-Brain Continuum: Sensory Processes , 1996 .

[126]  R. Nudo,et al.  Neural Substrates for the Effects of Rehabilitative Training on Motor Recovery After Ischemic Infarct , 1996, Science.

[127]  R. Dawkins Climbing Mount Improbable , 1996 .

[128]  M. Schieber Individuated Finger Movements: Rejecting the Labeled-Line Hypothesis , 1996 .

[129]  J C Rothwell,et al.  Abnormal access of axial vibrotactile input to deafferented somatosensory cortex in human upper limb amputees. , 1997, Journal of neurophysiology.

[130]  J. Kaas,et al.  Mechanisms of reorganization in sensory systems of primates after peripheral nerve injury. , 1997, Advances in neurology.

[131]  Filling in gaps in perception: Part II. Scotomas and phantom limbs , 1997 .

[132]  V. Ramachandran,et al.  Capgras syndrome: a novel probe for understanding the neural representation of the identity and familiarity of persons , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[134]  V. Ramachandran,et al.  Acute plasticity in the human somatosensory cortex following amputation , 1998, Neuroreport.

[135]  V. Ramachandran,et al.  The perception of phantom limbs , 1998 .

[136]  V. Ramachandran,et al.  Three Laws of Qualia , 1999 .