Long-term motor cortex plasticity induced by an electronic neural implant

It has been proposed that the efficacy of neuronal connections is strengthened when there is a persistent causal relationship between presynaptic and postsynaptic activity. Such activity-dependent plasticity may underlie the reorganization of cortical representations during learning, although direct in vivo evidence is lacking. Here we show that stable reorganization of motor output can be induced by an artificial connection between two sites in the motor cortex of freely behaving primates. An autonomously operating electronic implant used action potentials recorded on one electrode to trigger electrical stimuli delivered at another location. Over one or more days of continuous operation, the output evoked from the recording site shifted to resemble the output from the corresponding stimulation site, in a manner consistent with the potentiation of synaptic connections between the artificially synchronized populations of neurons. Changes persisted in some cases for more than one week, whereas the output from sites not incorporated in the connection was unaffected. This method for inducing functional reorganization in vivo by using physiologically derived stimulus trains may have practical application in neurorehabilitation after injury.

[1]  O. L. Z. Book Review: The Organization of Behaviour: A Neuropsychological Theory , 1950 .

[2]  E Jankowska,et al.  The mode of activation of pyramidal tract cells by intracortical stimuli. , 1975, The Journal of physiology.

[3]  A. Baranyi,et al.  Synaptic facilitation requires paired activation of convergent pathways in the neocortex , 1981, Nature.

[4]  Masao Ito,et al.  Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex , 1982, Neuroscience Letters.

[5]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[6]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[7]  M. Dowd,et al.  An ongoing debate. , 1988, Geriatric nursing.

[8]  A. Keller,et al.  Long-term potentiation in the motor cortex. , 1989, Science.

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

[10]  E. Fetz,et al.  Synaptic Interactions between Cortical Neurons , 1991 .

[11]  M. Ahissar,et al.  Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. , 1992, Science.

[12]  Norton W. Milgram,et al.  Post-activation potentiation in the neocortex. IV. Multiple sessions required for induction of long-term potentiation in the chronic preparation , 1995, Brain Research.

[13]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  J. Donoghue,et al.  Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. , 1996, Journal of neurophysiology.

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

[16]  P. Milner,et al.  Preconceptions and prerequisites: Understanding the function of synaptic plasticity will also depend on a better systems-level understanding of the multiple types of memory , 1997, Behavioral and Brain Sciences.

[17]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[18]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[19]  J. Kleim,et al.  Functional reorganization of the rat motor cortex following motor skill learning. , 1998, Journal of neurophysiology.

[20]  L. Paninski,et al.  Information about movement direction obtained from synchronous activity of motor cortical neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Donoghue,et al.  Neuronal Interactions Improve Cortical Population Coding of Movement Direction , 1999, The Journal of Neuroscience.

[22]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[23]  Martin E. Schwab,et al.  Plasticity of motor systems after incomplete spinal cord injury , 2001, Nature Reviews Neuroscience.

[24]  R. C. Tees Review of The organization of behavior: A neuropsychological theory. , 2003 .

[25]  A. Jackson,et al.  Synchrony between Neurons with Similar Muscle Fields in Monkey Motor Cortex , 2003, Neuron.

[26]  Ann M. Stowe,et al.  Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: A feasibility study in primates , 2003, Neurological research.

[27]  Y. Dan,et al.  Spike Timing-Dependent Plasticity of Neural Circuits , 2004, Neuron.

[28]  J. Kleim,et al.  Long-term potentiation induces expanded movement representations and dendritic hypertrophy in layer V of rat sensorimotor neocortex. , 2004, Cerebral cortex.

[29]  E. Kandel,et al.  A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Rothwell,et al.  Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke , 2005, Neurology.

[31]  Marie-H Monfils,et al.  In Search of the Motor Engram: Motor Map Plasticity as a Mechanism for Encoding Motor Experience , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[32]  R. Stickgold,et al.  Sleep and memory: the ongoing debate. , 2005, Sleep.

[33]  Andrew Jackson,et al.  An autonomous implantable computer for neural recording and stimulation in unrestrained primates , 2005, Journal of Neuroscience Methods.

[34]  E. Fetz,et al.  The neurochip BCI: towards a neural prosthesis for upper limb function , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[35]  M. Poo,et al.  Spike Timing-Dependent LTP/LTD Mediates Visual Experience-Dependent Plasticity in a Developing Retinotectal System , 2006, Neuron.

[36]  E. Fetz,et al.  Correlations between the same motor cortex cells and arm muscles during a trained task, free behavior, and natural sleep in the macaque monkey. , 2007, Journal of neurophysiology.