Skip to main content
Log in

A neural network model of phantom limbs

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

This paper presents a detailed clinical description of phantom limbs and a neuronal network model that provides a comprehensive and parsimonious explanation of otherwise inexplicable or at least unrelated phenomena. Simulations of self-organizing feature maps (Kohonen networks) that had been trained to recognize input patterns were deprived of parts of their input in order to simulate partial deafferentation. This leads to reorganization processes that are shown to be driven by input noise. In patients with an amputated limb, this noise is generated by dorsal root ganglion sensory neurons which are known to fire irregularly upon laceration. According to this model, the long-standing debate concerning non-cortical vs. cortical contributions to the generation of the phenomenon of phantom limbs can be resolved in that it is the peripherally generated noise that causes cortical reorganization. The model can be tested and may have therapeutic implications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson JA, Pellionisz A, Rosenfeld E (1990) Introduction (to chapters 17,18, and 19). In: Anderson JA, Pellionisz A, Rosenfeld E (eds) Neurocomputing 2. Directions for research. MIT Press, Cambridge, Mass. pp 295–299

    Google Scholar 

  • Antonini A, Stryker MP (1993) Rapid remodeling of axonal arbors in the visual cortex. Science 260:1819–1821

    Google Scholar 

  • Bach y Rita P (1990) Brain plasticity as a basis for recovery of function in humans. Neuropsychologia 28:547–554

    Google Scholar 

  • Bors E (1951) Phantom limbs of patients with spinal cord injury. Arch Neurol Psychiatr 66:610–631

    Google Scholar 

  • Buchanen DC, Mandel AR (1986) The prevalence of phantom limb experience in amputees. Rehab Psychol 31:183–188

    Google Scholar 

  • Carlen PL, Wall PD, Nadvorna H, Steinbach T (1978) Phantom limbs and related phenomena in recent traumatic amputations. Neurology 28:211–217

    Google Scholar 

  • Caudill M, Butler C (1992) Understanding neural networks, Vols 1 and 2. MIT Press, Cambridge, Mass

    Google Scholar 

  • Changeux J-P, Heidmann T, Patte P (1984) Learning by selection. In: Marker P, Terrence HS (eds) The biology of learning. Springer, Berlin Heidelberg New York [Quoted from: pp 115–133 Rosenfeld E, Pellionisz A, Anderson JA (eds) (1990) Neurocomputing 2. Directions for research. MIT Press, Cambridge, Mass. pp 300–307

    Google Scholar 

  • Churchland PS, Koch C, Sejnowski TJ (1990) What is computational neuroscience? In: Schwartz EL (eds) Computational neuroscience. MIT Press, Cambridge, Mass. pp 38–45

    Google Scholar 

  • Cohen J, Servan-Schreiber D (1992) Context, cortex and dopamine: a connectionist approach to behavior and biology in schizophrenia. Psychol Rev 12:45–77

    Google Scholar 

  • Creutzfeld DO (1993) Cortex cerebri. Sellstverlag Göttingen

    Google Scholar 

  • Crick F (1988) What mad pursuit. Basic Books, New York

    Google Scholar 

  • Crick F (1989) The recent excitement about neural networks. Nature 337:129–132

    Google Scholar 

  • Cronholm B (1951) Phantom limbs in amputees. Acta Psychiatr Neurol Scand Suppl 72:1–310

    Google Scholar 

  • Devor M (1984) The pathophysiology and anatomy of damaged nerve. In: Wall PD, Melzak M (eds) Textbook of pain. Churchill-Livingstone, Edinburgh, pp 49–64

    Google Scholar 

  • Douglas JK, Wilkens L, Pantazelou E, Moss F (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365:337–340

    Google Scholar 

  • Edelman GM, Finkel LH (1984) Neuronal group selection in the cerebral cortex. In: Edelman GM, Einar-Gall W, Maxwell W (eds) Dynamic aspects of neocortical function. Wiley-Interscience, New York, pp 653–595 [Quoted from: Anderson, JA, Pellionisz, A Rosenfeld E (ed) (1990) Neurocomputing 2. Directions for research. MIT Press, Cambridge, Mass. pp 308–334

    Google Scholar 

  • Gilbert CD (1993) Rapid dynamic changes in adult cerebral cortex. Curr Opin Neurobiol 3:100–103

    Google Scholar 

  • Halligan PW, Marshall JC, Wade DT, Davey J, Morrison D (1993) Thumb in cheek? Sensory reorganization and perceptual plasticity after limb amputation. Neuroreport 4:233–236

    Google Scholar 

  • Hoffman J (1954) Phantom limb syndrome. A critical review of the literature. J Nerv Ment Dis 119:261–270

    Google Scholar 

  • Jensen TS, Rasmussen P (1989) Phantom pain and related phenomena after amputation. In: Wall PD, Melzack R (eds) Textbook of pain, 2nd edn Livingstone Churchill, Edinburgh

    Google Scholar 

  • Jensen TS, Krebs B, Nielsen J, Rasmussen P (1984) Non-painful phantom limb phenomena in amputees: incidence, clinical characteristics and temporal course. Acta Neurol Scand 70:407–414

    Google Scholar 

  • Katz J (1992) Psychophysiological contributions to phantom limbs. Can J Psychiatry 37:282–298

    Google Scholar 

  • Kohonen T (1982) Self-organized formation of topologically correct feature maps. Biol Cybern 43:59–69

    Google Scholar 

  • Kohonen T (1989) Self-organization and associative memory, 3rd edn Springer, Berlin Heidelberg New York

    Google Scholar 

  • Kosslyn S, Koenig O (1992) Wet Mind. The New Cognitive Neuroscience. Macmillan, New York, Toronto, Oxford, Singapore, Sydney

    Google Scholar 

  • Maddox J (1994) Bringing more order out of noisiness. Nature 369:271

    Google Scholar 

  • Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D (1983) Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8:33–55

    Google Scholar 

  • Merzenich MM, Sameshima K (1993) Cortical plasticity and memory. Curr Opin Neurol 3:187–196

    Google Scholar 

  • Miikkulainen R (1993) Subsymbolic natural language processing. An integrated model of scripts, lexicon, and memory. MIT Press, Cambridge Mass.

    Google Scholar 

  • Mitchell SW (1871) Phantom limbs. Lippinocott Mag Pop Lit Sci 8:563–569

    Google Scholar 

  • Morrison JH, Hof PR (1992) The organization of cerebral cortex: from molecules to circuits. Discuss Neurosci 9:1–80

    Google Scholar 

  • Neumann von (1958) The computer and the brain. Yale University Press, New Haven

    Google Scholar 

  • O'Leary DDM (1992) Development of connectional diversity and specificity in the mammalian brain by the pruning of collateral projections. Curr Opin Neurobiol 2:70–77

    Google Scholar 

  • Penfield W, Rasmussen T (1950) The cerebral cortex of man: a clinical study of localization and function. Macmillan, New York

    Google Scholar 

  • Poeck K (1963) Zur Psychophysiologie der Phantomerlebnisse. Nervenarzt 34:241–256

    Google Scholar 

  • Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M (1991) Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252:1857–1860

    Google Scholar 

  • Ramachandran VS, Rogers-Ramachandran D, Steward M (1992) Perceptual correlates of massive cortical reorganization. Science 258:1159–1160

    Google Scholar 

  • Recanzone GH, Jenkins WM, Hradek GT, Merzenich MM (1992a) rogressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task. J Neurophysiol 67:1015–1030

    Google Scholar 

  • Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR (1992b) Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency-discrimination task. Neuroiphysiol 67:1031–1056

    Google Scholar 

  • Recanzone GH, Merzenich MM, Schreiner CE (1992c) Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. J Neurophysiol 67:1071–1091

    Google Scholar 

  • Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 13:87–103

    Google Scholar 

  • Ritter H (1991) Neuronale Netze. Addison-Wesley, Reading

    Google Scholar 

  • Ritter H, Kohonen T (1989) Self-organizing semantic maps. Biol Cybern 61:241–254

    Google Scholar 

  • Rumelhart D (1989) The architecture of mind: A connectionist approach. In: Posner M (eds) Foundations of Cognitive Science. MIT Press, Cambridge, Mass. pp 133–159

    Google Scholar 

  • Schilder P (1923) Über elementate Halluzinationen des Bewegungssehens. Z Neurol Psychiatrie 80:424–431

    Google Scholar 

  • Shepherd GM (1990) The significance of real neuron architectures for neural network simulations. In: Schwartz EL (ed) Computational neuroscience. MIT Press, Cambridge, Mass. pp 82–96

    Google Scholar 

  • Spitzer M (1988) Halluzinationen. Springer. Berlin Heidelberg New York

    Google Scholar 

  • Spitzer M, Braun U, Hermle L, Maier S (1993) Associative semantic network dysfunction in thought-disordered schizophrenic patients: direct evidence from indirect semantic priming. Biol. Psychiatry 34:864–877

    Google Scholar 

  • Sutton G, Reggia J, Armentrout S, D'Autrechy C (1994) Cortical map reorganization as a competitive process. Neural Comp 6:1–13

    Google Scholar 

  • Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex Trends Neuro Sci 17:119–126

    Google Scholar 

  • Weinstein S, Sersen EA, Vetter RJ (1964) Phantoms and somatic sensation in cases of congenital aplasia. Neurology 10:905–911

    Google Scholar 

  • Weiss SA, Fishman S (1963) Extended and telescoped phantom limbs in unilateral amputees. l J Abnorm Soc Psychol 66:489–497

    Google Scholar 

  • Welk E, Leah JD, Zimmermann M (1990) Characteristics of A- and C-fibers ending in a sensory nerve neuroma in the rat. J. Neurophysiol 63:759–766

    Google Scholar 

  • Zuk GH (1956) The phantom limb: a proposed theory of unconscious origins. J Nerv Ment Dis 124:510–513

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spitzer, M., Böhler, P., Weisbrod, M. et al. A neural network model of phantom limbs. Biol. Cybern. 72, 197–206 (1995). https://doi.org/10.1007/BF00201484

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00201484

Keywords

Navigation