Microstimulation of V1 delays the execution of visually guided saccades

Electrical stimulation delivered to V1 concurrently with the presentation of a visual target interferes with both the selection and the detection of targets positioned in the receptive field of the stimulated neurons. In the present study, we examined the temporal course of this effect by delivering electrical stimulation to V1 of rhesus monkeys at various times before the appearance of a visual target. Each trial was initiated by the appearance of a fixation spot that, once acquired, was followed by the presentation of a visual target in the receptive field of the stimulated neurons. A monkey was reward after making a saccadic eye movement to the target. A delay in saccade generation was obtained when stimulation was delivered while an animal maintained fixation on the fixation spot. No delay occurred when the visual target was placed outside the receptive field of the stimulated neurons. The best parameters for inducing the saccadic delay were: (i) anode‐first pulses (as opposed to cathode‐first pulses) and (ii) train durations greater than 40 ms and frequencies greater than 100 Hz. The lowest current threshold for producing a saccadic delay occurred at 1.5 mm below the top of superficial V1. The chronaxies of the directly stimulated elements mediating the delay ranged from 0.13 to 0.24 ms. These values overlap with those that have been described for phosphene induction in human V1. We discuss how the elements mediating the saccadic delay might interrupt a visual signal as it passes along the geniculostriate pathway.

[1]  R. Wurtz,et al.  What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. , 2004, Journal of neurophysiology.

[2]  Peter H Schiller,et al.  Cortical inhibitory circuits in eye‐movement generation , 2003, The European journal of neuroscience.

[3]  David Bradley,et al.  A model for intracortical visual prosthesis research. , 2003, Artificial organs.

[4]  N. Logothetis,et al.  Simultaneous electrical microstimulation and fMRI in the macaque , 2003 .

[5]  Christina E Carvey,et al.  Behavioural state affects saccadic eye movements evoked by microstimulation of striate cortex , 2003, The European journal of neuroscience.

[6]  E. J. Tehovnik,et al.  Using ocular dominance to infer the depth of the visual input layers of V1 in behaving macaque monkey , 2003, Journal of Neuroscience Methods.

[7]  E. J. Tehovnik,et al.  Saccadic eye movements evoked by microstimulation of striate cortex , 2003, The European journal of neuroscience.

[8]  J. Duhamel,et al.  Saccadic Target Selection Deficits after Lateral Intraparietal Area Inactivation in Monkeys , 2002, The Journal of Neuroscience.

[9]  E. J. Tehovnik,et al.  Differential effects of laminar stimulation of V1 cortex on target selection by macaque monkeys , 2002, The European journal of neuroscience.

[10]  Warren M. Grill,et al.  Selective Microstimulation of Central Nervous System Neurons , 2000, Annals of Biomedical Engineering.

[11]  F. Rattay,et al.  The basic mechanism for the electrical stimulation of the nervous system , 1999, Neuroscience.

[12]  D. Ferster,et al.  Strength and Orientation Tuning of the Thalamic Input to Simple Cells Revealed by Electrically Evoked Cortical Suppression , 1998, Neuron.

[13]  J. Bullier,et al.  Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter I. Evidence from chronaxie measurements , 1998, Experimental Brain Research.

[14]  Marc A. Sommer,et al.  Electrically evoked saccades from the dorsomedial frontal cortex and frontal eye fields: a parametric evaluation reveals differences between areas , 1997, Experimental Brain Research.

[15]  E. J. Tehovnik,et al.  Excitability of neural elements within the rat corpus striatum , 1997, Journal of Neuroscience Methods.

[16]  C. Kufta,et al.  Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. , 1996, Brain : a journal of neurology.

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

[18]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[19]  S. Levay,et al.  The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  W. Fries Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase , 1984, The Journal of comparative neurology.

[21]  H. Fields,et al.  Relations among threshold, spike height, electrode distance, and conduction velocity in electrical stimulation of certain medullospinal neurons. , 1984, Journal of neurophysiology.

[22]  D. C. West,et al.  Strength‐duration characteristics of myelinated and non‐myelinated bulbospinal axons in the cat spinal cord. , 1983, The Journal of physiology.

[23]  M. Colonnier,et al.  A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys , 1982, The Journal of comparative neurology.

[24]  J. Mcilwain Lateral spread of neural excitation during microstimulation in intermediate gray layer of cat's superior colliculus. , 1982, Journal of neurophysiology.

[25]  D. Pollen,et al.  Intracortical microstimulation of neurons in the visual cortex of the cat. , 1981, Electroencephalography and clinical neurophysiology.

[26]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[27]  T. Powell,et al.  The basic uniformity in structure of the neocortex. , 1980, Brain : a journal of neurology.

[28]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[29]  J. Malpeli,et al.  Shock-induced inhibition in the lateral geniculate nucleus of the rhesus monkey , 1977, Brain Research.

[30]  G. Matthews Neural substrate for brain stimulation reward in the rat: cathodal and anodal strength-duration properties. , 1977, Journal of comparative and physiological psychology.

[31]  A. Arnold,et al.  Further study on the excitation of pyramidal tract cells by intracortical microstimulation , 1976, Experimental Brain Research.

[32]  B L Finlay,et al.  Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. , 1976, Journal of neurophysiology.

[33]  C. Li,et al.  Excitability characteristics of the A- and C-fibers in a peripheral nerve , 1976, Experimental Neurology.

[34]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

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

[36]  D. Hubel,et al.  The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain , 1975, The Journal of comparative neurology.

[37]  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.

[38]  D H Hubel,et al.  Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. , 1974, Brain research.

[39]  W. Roberts,et al.  Analysis of threshold currents during microstimulation of fibres in the spinal cord. , 1973, Acta physiologica Scandinavica.

[40]  D. Armstrong,et al.  The spatial organisation of climbing fibre branching in the cat cerebellum , 1973, Experimental Brain Research.

[41]  E. Jankowska,et al.  An electrophysiological demonstration of the axonal projections of single spinal interneurones in the cat , 1972, The Journal of physiology.

[42]  W. D. Thompson,et al.  Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. , 1968, Journal of neurophysiology.

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

[44]  Brindley Gs,et al.  The visual sensations produced by electrical stimulation of the medial occipital cortex. , 1968, The Journal of physiology.

[45]  B. Cragg The density of synapses and neurones in the motor and visual areas of the cerebral cortex. , 1967, Journal of anatomy.

[46]  R. Porter,et al.  Focal stimulation of hypoglossal neurones in the cat , 1963, The Journal of physiology.

[47]  O. Oscarsson,et al.  The lateral reticular nucleus in the cat I. Mossy fibre distribution in cerebellar cortex , 2004, Experimental Brain Research.

[48]  Edward J. Tehovnik,et al.  The dorsomedial frontal cortex of the rhesus monkey: topographic representation of saccades evoked by electrical stimulation , 2004, Experimental Brain Research.

[49]  C. Ekerot The lateral reticular nucleus in the cat , 2004, Experimental Brain Research.

[50]  E. J. Tehovnik,et al.  Microstimulation of macaque V1 disrupts target selection: effects of stimulation polarity , 2002, Experimental Brain Research.

[51]  P H Schiller,et al.  Look and see: how the brain moves your eyes about. , 2001, Progress in brain research.

[52]  A. Peters Number of Neurons and Synapses in Primary Visual Cortex , 1987 .

[53]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[54]  I. Khalilov,et al.  Early sequential formation of functional GABAA and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus , 2002, The European journal of neuroscience.