Probing neural circuitry and function with electrical microstimulation

Since the discovery of the nervous system's electrical excitability more than 200 years ago, neuroscientists have used electrical stimulation to manipulate brain activity in order to study its function. Microstimulation has been a valuable technique for probing neural circuitry and identifying networks of neurons that underlie perception, movement and cognition. In this review, we focus on the use of stimulation in behaving primates, an experimental system that permits causal inferences to be made about the effect of stimulation-induced activity on the resulting behaviour or neural signals elsewhere in the brain.

[1]  N. Logothetis,et al.  The effects of electrical microstimulation on cortical signal propagation , 2010, Nature Neuroscience.

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

[3]  Michael Brecht,et al.  Nanostimulation: manipulation of single neuron activity by juxtacellular current injection. , 2010, Journal of neurophysiology.

[4]  Zador Anthony Differential sensitivity of different sensory cortices to behaviorally relevant timing differences , 2010 .

[5]  R. Reid,et al.  Direct Activation of Sparse, Distributed Populations of Cortical Neurons by Electrical Microstimulation , 2009, Neuron.

[6]  P. Roelfsema,et al.  Modulation of the Contrast Response Function by Electrical Microstimulation of the Macaque Frontal Eye Field , 2009, The Journal of Neuroscience.

[7]  O. Devinsky,et al.  The excitable cerebral cortex: Fritsch G, Hitzig E. Über die elektrische Erregbarkeit des Grosshirns. Arch Anat Physiol Wissen 1870;37:300–32. , 2009, Epilepsy & Behavior.

[8]  Anthony M Zador,et al.  Millisecond-scale differences in neural activity in auditory cortex can drive decisions , 2008, Nature Neuroscience.

[9]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

[10]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[11]  John H R Maunsell,et al.  Electrical microstimulation thresholds for behavioral detection and saccades in monkey frontal eye fields , 2008, Proceedings of the National Academy of Sciences.

[12]  T. Sejnowski,et al.  Regulation of spike timing in visual cortical circuits , 2008, Nature Reviews Neuroscience.

[13]  Arthur R. Houweling,et al.  Behavioural report of single neuron stimulation in somatosensory cortex , 2008, Nature.

[14]  Tirin Moore,et al.  Attention Governs Action in the Primate Frontal Eye Field , 2007, Neuron.

[15]  Tirin Moore,et al.  Temporal Patterning of Saccadic Eye Movement Signals , 2007, The Journal of Neuroscience.

[16]  Tirin Moore,et al.  Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field , 2007, Proceedings of the National Academy of Sciences.

[17]  John H.R. Maunsell,et al.  Behavioral Detection of Electrical Microstimulation in Different Cortical Visual Areas , 2007, Current Biology.

[18]  K. Shenoy,et al.  Delay of movement caused by disruption of cortical preparatory activity. , 2007, Journal of neurophysiology.

[19]  E. Fetz,et al.  Long-term motor cortex plasticity induced by an electronic neural implant , 2006, Nature.

[20]  G. Feng,et al.  Next-Generation Optical Technologies for Illuminating Genetically Targeted Brain Circuits , 2006, The Journal of Neuroscience.

[21]  R. Kiani,et al.  Microstimulation of inferotemporal cortex influences face categorization , 2006, Nature.

[22]  E. J. Tehovnik,et al.  Direct and indirect activation of cortical neurons by electrical microstimulation. , 2006, Journal of neurophysiology.

[23]  Timothy D. Hanks,et al.  Microstimulation of macaque area LIP affects decision-making in a motion discrimination task , 2006, Nature Neuroscience.

[24]  Ziv M. Williams,et al.  Selective enhancement of associative learning by microstimulation of the anterior caudate , 2006, Nature Neuroscience.

[25]  C. Gross,et al.  Representations of faces and body parts in macaque temporal cortex: a functional MRI study. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Robert H. Wurtz,et al.  Subcortical Modulation of Attention Counters Change Blindness , 2004, The Journal of Neuroscience.

[27]  W. Singer,et al.  Amplitude and direction of saccadic eye movements depend on the synchronicity of collicular population activity. , 2004, Journal of neurophysiology.

[28]  M. Graziano,et al.  Mapping from motor cortex to biceps and triceps altered by elbow angle. , 2004, Journal of neurophysiology.

[29]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[30]  W. Newsome,et al.  What electrical microstimulation has revealed about the neural basis of cognition , 2004, Current Opinion in Neurobiology.

[31]  V. Ferrera,et al.  Modification of Saccades Evoked by Stimulation of Frontal Eye Field during Invisible Target Tracking , 2004, The Journal of Neuroscience.

[32]  P. Schiller,et al.  Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey , 2004, Experimental Brain Research.

[33]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[34]  C. Gross,et al.  Twitches Versus Movements: A Story of Motor Cortex , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[35]  Doris Y. Tsao,et al.  Faces and objects in macaque cerebral cortex , 2003, Nature Neuroscience.

[36]  M. Shadlen,et al.  Microstimulation of visual cortex affects the speed of perceptual decisions , 2003, Nature Neuroscience.

[37]  Tirin Moore,et al.  Complex movements evoked by microstimulation of the ventral intraparietal area , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Gold,et al.  The Influence of Behavioral Context on the Representation of a Perceptual Decision in Developing Oculomotor Commands , 2003, The Journal of Neuroscience.

[39]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

[40]  M. Graziano,et al.  Complex Movements Evoked by Microstimulation of Precentral Cortex , 2002, Neuron.

[41]  S. Lisberger,et al.  Enhancement of multiple components of pursuit eye movement by microstimulation in the arcuate frontal pursuit area in monkeys. , 2002, Journal of neurophysiology.

[42]  R. Wurtz,et al.  Interaction of the frontal eye field and superior colliculus for saccade generation. , 2001, Journal of neurophysiology.

[43]  T Moore,et al.  Control of eye movements and spatial attention. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Paul D. Gamlin,et al.  An area for vergence eye movement in primate frontal cortex , 2000, Nature.

[45]  J. Kalaska,et al.  Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. , 2000, Journal of neurophysiology.

[46]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[47]  E. J. Tehovnik,et al.  Eye fields in the frontal lobes of primates , 2000, Brain Research Reviews.

[48]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

[49]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[50]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[51]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[52]  Wolf Singer,et al.  Time as coding space? , 1999, Current Opinion in Neurobiology.

[53]  R. Andersen,et al.  Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. , 1998, Journal of neurophysiology.

[54]  E. Seidemann,et al.  Temporal gating of neural signals during performance of a visual discrimination task , 1998, Nature.

[55]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[56]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

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

[58]  C. Bruce,et al.  Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. , 1997, Journal of neurophysiology.

[59]  J. Schall Visuomotor Areas of the Frontal Lobe , 1997 .

[60]  D. Robinson,et al.  Shared neural control of attentional shifts and eye movements , 1996, Nature.

[61]  D. Sparks,et al.  Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. , 1996, Journal of neurophysiology.

[62]  E. J. Tehovnik Electrical stimulation of neural tissue to evoke behavioral responses , 1996, Journal of Neuroscience Methods.

[63]  K. Rockland,et al.  Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. , 1993, Cerebral cortex.

[64]  C. Bruce,et al.  Smooth eye movements elicited by microstimulation in the primate frontal eye field. , 1993, Journal of neurophysiology.

[65]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[66]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[67]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. , 1985, Journal of neurophysiology.

[68]  F. J. Clark,et al.  Microstimulation of single tactile afferents from the human hand. Sensory attributes related to unit type and properties of receptive fields. , 1984, Brain : a journal of neurology.

[69]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  S. Wise,et al.  A neurophysiological study of the premotor cortex in the rhesus monkey. , 1984, Brain : a journal of neurology.

[71]  R. Desimone,et al.  Columnar organization of directionally selective cells in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[72]  E. G. Keating,et al.  Removing the superior colliculus silences eye movements normally evoked from stimulation of the parietal and occipital eye fields , 1983, Brain Research.

[73]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[74]  D. Robinson Control of eye movements , 1981 .

[75]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

[76]  R. Doty,et al.  An exploration of the ability of macaques to detect microstimulation of striate cortex. , 1980, Acta Neurobiologiae Experimentalis.

[77]  Peter L. Strick,et al.  Multiple representation in the primate motor cortex , 1978, Brain Research.

[78]  E. Keller,et al.  Colliculoreticular organization in primate oculomotor system. , 1977, Journal of neurophysiology.

[79]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[80]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[81]  P. Schiller,et al.  Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. , 1972, Journal of neurophysiology.

[82]  A. Fuchs,et al.  Eye movements evoked by stimulation of frontal eye fields. , 1969, Journal of neurophysiology.

[83]  G. Brindley,et al.  The sensations produced by electrical stimulation of the visual cortex , 1968, The Journal of physiology.

[84]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[85]  A. Fuchs Saccadic and smooth pursuit eye movements in the monkey , 1967, The Journal of physiology.

[86]  H. Sakata,et al.  Functional Organization of a Cortical Efferent System Examined with Focal Depth Stimulation in Cats , 1967 .

[87]  W. Penfield The Excitable Cortex in Conscious Man , 1958 .

[88]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[89]  D. Ferrier The Functions of the Brain , 1887, Edinburgh Medical Journal.

[90]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .