Embedding a Panoramic Representation of Infrared Light in the Adult Rat Somatosensory Cortex through a Sensory Neuroprosthesis

Can the adult brain assimilate a novel, topographically organized, sensory modality into its perceptual repertoire? To test this, we implemented a microstimulation-based neuroprosthesis that rats used to discriminate among infrared (IR) light sources. This system continuously relayed information from four IR sensors that were distributed to provide a panoramic view of IR sources, into primary somatosensory cortex (S1). Rats learned to discriminate the location of IR sources in <4 d. Animals in which IR information was delivered in spatial register with whisker topography learned the task more quickly. Further, in animals that had learned to use the prosthesis, altering the topographic mapping from IR sensor to stimulating electrode had immediate deleterious effects on discrimination performance. Multielectrode recordings revealed that S1 neurons had multimodal (tactile/IR) receptive fields, with clear preferences for those stimuli most likely to be delivered during the task. Neuronal populations predicted, with high accuracy, which stimulation pattern was present in small (75 ms) time windows. Surprisingly, when identical microstimulation patterns were delivered during an unrelated task, cortical activity in S1 was strongly suppressed. Overall, these results show that the adult mammalian neocortex can readily absorb completely new information sources into its representational repertoire, and use this information in the production of adaptive behaviors. SIGNIFICANCE STATEMENT Understanding the potential for plasticity in the adult brain is a key goal for basic neuroscience and modern rehabilitative medicine. Our study examines one dimension of this challenge: how malleable is sensory processing in adult mammals? We implemented a panoramic infrared (IR) sensory prosthetic system in rats; it consisted of four IR sensors equally spaced around the circumference of the head of the rat. Each sensor was coupled to a microstimulating electrode placed in the somatosensory cortex of the rat. Within days, rats learned to use the prosthesis to track down items associated with IR light in their environment. This is quite promising clinically, as the largest demand for sensory prosthetic devices is in adults whose brains are already fully developed.

[1]  Arthur James Lowery,et al.  Restoration of vision in blind individuals using bionic devices: A review with a focus on cortical visual prostheses , 2015, Brain Research.

[2]  M. Sur,et al.  Visual behaviour mediated by retinal projections directed to the auditory pathway , 2000, Nature.

[3]  Nicolelis Mal.  Multielectrode Recordings in the Somatosensory System -- Methods for Neural Ensemble Recordings , 2008 .

[4]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[5]  Miguel A. L. Nicolelis,et al.  Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex , 1999, Nature Neuroscience.

[6]  Mikhail A. Lebedev,et al.  How to read neuron-dropping curves? , 2014, Front. Syst. Neurosci..

[7]  Peter König,et al.  Sensory Augmentation for the Blind , 2012, Front. Hum. Neurosci..

[8]  Richard A. Andersen,et al.  Toward More Versatile and Intuitive Cortical Brain–Machine Interfaces , 2014, Current Biology.

[9]  W. Dobelle,et al.  Phosphenes produced by electrical stimulation of human occipital cortex, and their application to the development of a prosthesis for the blind , 1974, The Journal of physiology.

[10]  D. Frost,et al.  Induction of functional retinal projections to the somatosensory system , 1985, Nature.

[11]  BENJAMIN WHITE,et al.  Vision Substitution by Tactile Image Projection , 1969, Nature.

[12]  Mikhail A Lebedev,et al.  Virtual Active Touch Using Randomly Patterned Intracortical Microstimulation , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[13]  M. Nicolelis,et al.  High-Side Digitally Current Controlled Biphasic Bipolar Microstimulator , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[14]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[15]  P. König,et al.  Beyond sensory substitution—learning the sixth sense , 2005, Journal of neural engineering.

[16]  Sabine U. König,et al.  The experience of new sensorimotor contingencies by sensory augmentation , 2014, Consciousness and Cognition.

[17]  Mei Zhang,et al.  Spinal Cord Stimulation Restores Locomotion in Animal Models of Parkinson ’ s Disease , 2009 .

[18]  M E Diamond,et al.  Distribution of tactile learning and its neural basis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Amol P. Yadav,et al.  Chronic Spinal Cord Electrical Stimulation Protects Against 6-hydroxydopamine Lesions , 2014, Scientific Reports.

[20]  Mohamad Sawan,et al.  A Highly Flexible System for Microstimulation of the Visual Cortex: Design and Implementation , 2007, IEEE Transactions on Biomedical Circuits and Systems.

[21]  George L. Gerstein,et al.  Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study , 1996, Experimental Brain Research.

[22]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[23]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[24]  Mriganka Sur,et al.  Visual activity and cortical rewiring: activity-dependent plasticity of cortical networks. , 2006, Progress in brain research.

[25]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[26]  Eric E. Thomson,et al.  Multielectrode Recordings in the Somatosensory System , 2008 .

[27]  A. Lozano,et al.  Deep Brain Stimulation for Treatment-Resistant Depression , 2005, Neuron.

[28]  Erika E. Fanselow,et al.  Thalamic bursting in rats during different awake behavioral states , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Sur,et al.  Experimentally induced visual projections into auditory thalamus and cortex. , 1988, Science.

[30]  Ulrike Richter,et al.  Spinal Cord Stimulation Alleviates Motor Deficits in a Primate Model of Parkinson Disease , 2014, Neuron.

[31]  M. Stryker,et al.  A Cortical Circuit for Gain Control by Behavioral State , 2014, Cell.

[32]  Jung-Kyong Kim,et al.  Generalized Learning of Visual-to-auditory Substitution in Sighted Individuals , 2008 .

[33]  Yuji Ikegaya,et al.  Visual Cortical Prosthesis with a Geomagnetic Compass Restores Spatial Navigation in Blind Rats , 2015, Current Biology.

[34]  M A Nicolelis,et al.  Bilateral Integration of Whisker Information in the Primary Somatosensory Cortex of Rats , 2001, The Journal of Neuroscience.

[35]  William M. Rabinowitz,et al.  Better speech recognition with cochlear implants , 1991, Nature.

[36]  Mikhail A Lebedev,et al.  Simultaneous Top-down Modulation of the Primary Somatosensory Cortex and Thalamic Nuclei during Active Tactile Discrimination , 2013, The Journal of Neuroscience.

[37]  M E Diamond,et al.  Learning through maps: functional significance of topographic organization in primary sensory cortex. , 1999, Journal of neurobiology.

[38]  Heather M. Hudson,et al.  Hijacking Cortical Motor Output with Repetitive Microstimulation , 2011, The Journal of Neuroscience.

[39]  Eric E. Thomson,et al.  Perceiving Invisible Light through a Somatosensory Cortical Prosthesis , 2013, Nature Communications.

[40]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[41]  N. Cohen,et al.  Cochlear Implants , 2000 .

[42]  M. Merzenich,et al.  Repetitive microstimulation alters the cortical representation of movements in adult rats. , 1990, Somatosensory & motor research.

[43]  G. Deuschl,et al.  A randomized trial of deep-brain stimulation for Parkinson's disease. , 2006, The New England journal of medicine.

[44]  S. Udin,et al.  Abnormal visual input leads to development of abnormal axon trajectories in frogs , 1983, Nature.

[45]  M. Nicolelis,et al.  Behavioral Properties of the Trigeminal Somatosensory System in Rats Performing Whisker-Dependent Tactile Discriminations , 2001, The Journal of Neuroscience.

[46]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[47]  W. H. Dobelle.  Artificial vision for the blind by connecting a television camera to the visual cortex. , 2000, ASAIO journal.

[48]  William M. Stern,et al.  Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex , 2007, Nature Neuroscience.

[49]  Miguel A L Nicolelis,et al.  Dynamic shifting in thalamocortical processing during different behavioural states† , 2002, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences.

[50]  L C Katz,et al.  Relationships between segregated afferents and postsynaptic neurones in the optic tectum of three-eyed frogs , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  Solaiman Shokur,et al.  A Brain-Machine Interface Enables Bimanual Arm Movements in Monkeys , 2013, Science Translational Medicine.

[52]  Amy M. Ni,et al.  Microstimulation Reveals Limits in Detecting Different Signals from a Local Cortical Region , 2010, Current Biology.

[53]  Gislin Dagnelie,et al.  Detection, eye–hand coordination and virtual mobility performance in simulated vision for a cortical visual prosthesis device , 2009, Journal of neural engineering.

[54]  G. Recanzone,et al.  Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation. , 1992, Cerebral cortex.

[55]  G. Stratton.  Some preliminary experiments on vision without inversion of the retinal image. , 1896 .

[56]  Christophe Blanchet,et al.  NMDA receptor–dependent metaplasticity at hippocampal mossy fiber synapses , 2011, Nature Neuroscience.

[57]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[58]  F. Sengpiel,et al.  Influence of experience on orientation maps in cat visual cortex , 1999, Nature Neuroscience.

[59]  T S Davis,et al.  Spatial and temporal characteristics of V1 microstimulation during chronic implantation of a microelectrode array in a behaving macaque , 2012, Journal of neural engineering.