Revealing the neural fingerprints of a missing hand

The hand area of the primary somatosensory cortex contains detailed finger topography, thought to be shaped and maintained by daily life experience. Here we utilise phantom sensations and ultra high-field neuroimaging to uncover preserved, though latent, representation of amputees’ missing hand. We show that representation of the missing hand’s individual fingers persists in the primary somatosensory cortex even decades after arm amputation. By demonstrating stable topography despite amputation, our finding questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost. The discovery of persistent digit topography of amputees’ missing hand could be exploited for the development of intuitive and fine-grained control of neuroprosthetics, requiring neural signals of individual digits. DOI: http://dx.doi.org/10.7554/eLife.15292.001

[1]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[2]  M. Devor,et al.  Peripheral nervous system origin of phantom limb pain , 2014, PAIN®.

[3]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[4]  Jon H. Kaas,et al.  Large-Scale Reorganization in the Somatosensory Cortex and Thalamus after Sensory Loss in Macaque Monkeys , 2008, The Journal of Neuroscience.

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

[6]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[7]  N. Jain,et al.  Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries , 2015, The Journal of Neuroscience.

[8]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[9]  Karl J. Friston,et al.  Comparing the similarity and spatial structure of neural representations: A pattern-component model , 2011, NeuroImage.

[10]  E. Zohary,et al.  Topographic Representation of the Human Body in the Occipitotemporal Cortex , 2010, Neuron.

[11]  Lee E Miller,et al.  Responses of somatosensory area 2 neurons to actively and passively generated limb movements. , 2013, Journal of neurophysiology.

[12]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[13]  J. Kaas,et al.  A Histologically Visible Representation of the Fingers and Palm in Primate Area 3 b and its Immutability Following Long-term , 1998 .

[14]  L. Miller,et al.  Restoring sensorimotor function through intracortical interfaces: progress and looming challenges , 2014, Nature Reviews Neuroscience.

[15]  M. Corballis Comparing a single case with a control sample: Refinements and extensions , 2009, Neuropsychologia.

[16]  K. Reilly,et al.  Persistent hand motor commands in the amputees' brain. , 2006, Brain : a journal of neurology.

[17]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[18]  J. Diedrichsen,et al.  Hand use predicts the structure of representations in sensorimotor cortex , 2015, Nature Neuroscience.

[19]  J R Goldsmith,et al.  Statistical Evidence. , 1961, Science.

[20]  K. Reilly,et al.  Disentangling motor execution from motor imagery with the phantom limb. , 2012, Brain : a journal of neurology.

[21]  Zoltan Dienes,et al.  Using Bayes to get the most out of non-significant results , 2014, Front. Psychol..

[22]  K. Reilly,et al.  The moving phantom: Motor execution or motor imagery? , 2012, Cortex.

[23]  Angela Sirigu,et al.  The Motor Cortex and Its Role in Phantom Limb Phenomena , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[24]  K. Hagbarth,et al.  Microelectrode recordings from transected nerves in amputees with phantom limb pain , 1981, Neuroscience Letters.

[25]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[26]  H. Johansen-Berg,et al.  Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation , 2015, Brain : a journal of neurology.

[27]  Scott H Frey,et al.  Compensatory Changes Accompanying Chronic Forced Use of the Nondominant Hand by Unilateral Amputees , 2014, The Journal of Neuroscience.

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

[29]  Denis Schluppeck,et al.  Single-subject fMRI mapping at 7 T of the representation of fingertips in S1: a comparison of event-related and phase-encoding designs. , 2013, Journal of neurophysiology.

[30]  Niranjan Kambi,et al.  Large-scale reorganization of the somatosensory cortex following spinal cord injuries is due to brainstem plasticity , 2014, Nature Communications.

[31]  S. Francis,et al.  Mapping human somatosensory cortex in individual subjects with 7 T functional MRI 1 Running title : Mapping human somatosensory cortex , 2010 .

[32]  M. Sereno,et al.  A human parietal face area contains aligned head-centered visual and tactile maps , 2006, Nature Neuroscience.

[33]  M. Sereno,et al.  Fine-Grained Nociceptive Maps in Primary Somatosensory Cortex , 2012, The Journal of Neuroscience.

[34]  David W. Franklin,et al.  Computational Mechanisms of Sensorimotor Control , 2011, Neuron.

[35]  R. Treede,et al.  Quantitative sensory testing: a comprehensive protocol for clinical trials , 2006, European journal of pain.

[36]  Nathalie Richard,et al.  Primary motor cortex changes after amputation correlate with phantom limb pain and the ability to move the phantom limb , 2016, NeuroImage.

[37]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[38]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[39]  N. Logothetis,et al.  Lack of long-term cortical reorganization after macaque retinal lesions , 2005, Nature.

[40]  I. Douven,et al.  Rationality: a social-epistemology perspective , 2014, Front. Psychol..

[41]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[42]  Amir Amedi,et al.  New Whole-Body Sensory-Motor Gradients Revealed Using Phase-Locked Analysis and Verified Using Multivoxel Pattern Analysis and Functional Connectivity , 2015, The Journal of Neuroscience.

[43]  M. Lee,et al.  Statistical Evidence in Experimental Psychology , 2011, Perspectives on psychological science : a journal of the Association for Psychological Science.

[44]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[45]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[46]  Heidi Johansen-Berg,et al.  Phantom pain is associated with preserved structure and function in the former hand area , 2013, Nature Communications.

[47]  J. Kaas,et al.  A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations. , 1998, Cerebral cortex.

[48]  Steen Moeller,et al.  Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project , 2013, NeuroImage.

[49]  Heidi Johansen-Berg,et al.  Investigating the Stability of Fine-Grain Digit Somatotopy in Individual Human Participants , 2016, The Journal of Neuroscience.

[50]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[51]  Frans W Cornelissen,et al.  Large-scale remapping of visual cortex is absent in adult humans with macular degeneration , 2011, Nature Neuroscience.

[52]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[53]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[54]  K. Hagbarth,et al.  Ectopic sensory discharges and paresthesiae in patients with disorders of peripheral nerves, dorsal roots and dorsal columns , 1984, Pain.

[55]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

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

[57]  T. Aflalo,et al.  Mapping Behavioral Repertoire onto the Cortex , 2007, Neuron.

[58]  Heidi Johansen-Berg,et al.  Deprivation-related and use-dependent plasticity go hand in hand , 2013, eLife.