Perceiving Electrical Stimulation of Identified Human Visual Areas

We studied whether detectable percepts could be produced by electrical stimulation of intracranial electrodes placed over human visual areas identified with fMRI. Identification of areas was confirmed by recording local-field potentials from the electrode, such as face-selective electrical responses from electrodes over the fusiform face area (FFA). The probability of detecting electrical stimulation of a visual area varied with the position of the area in the visual cortical hierarchy. Stimulation of early visual areas including V1, V2, and V3 was almost always detected, whereas stimulation of late visual areas such as FFA was rarely detected. When percepts were elicited from late areas, subjects reported that they were simple shapes and colors, similar to the descriptions of percepts from early areas. There were no reports of elaborate percepts, such as faces, even in areas like FFA, where neurons have complex response properties. For sites eliciting percepts, the detection threshold was determined by varying the stimulation current as subjects performed a forced-choice detection task. Current thresholds were similar for late and early areas. The similarity between both percept quality and threshold across early and late areas suggests the presence of functional microcircuits that link electrical stimulation with perception.

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

[2]  W. Penfield SOME MECHANISMS OF CONSCIOUSNESS DISCOVERED DURING ELECTRICAL STIMULATION OF THE BRAIN. , 1958, Proceedings of the National Academy of Sciences of the United States of America.

[3]  I. Kaufman The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1951 .

[4]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[5]  G. Loeb,et al.  Visual sensations produced by intracortical microstimulation of the human occipital cortex , 1990, Medical and Biological Engineering and Computing.

[6]  S. C. Hong,et al.  Mapping of functional organization in human visual cortex , 2000, Neurology.

[7]  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.

[8]  E. J. Tehovnik,et al.  Mapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque , 2005, Neuron.

[9]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[10]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

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

[13]  B. Argall,et al.  Simplified intersubject averaging on the cortical surface using SUMA , 2006, Human brain mapping.

[14]  M. Beauchamp,et al.  Perception Matches Selectivity in the Human Anterior Color Center , 2008, Current Biology.

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

[16]  L. Merabet,et al.  Development of a cortical visual neuroprosthesis for the blind: the relevance of neuroplasticity , 2005, Journal of neural engineering.

[17]  Frank Tong,et al.  Cognitive neuroscience: Primary visual cortex and visual awareness , 2003, Nature Reviews Neuroscience.

[18]  Daniel Yoshor,et al.  Computer-controlled electrical stimulation for quantitative mapping of human cortical function. , 2009, Journal of neurosurgery.

[19]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[20]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[21]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[22]  E. J. Tehovnik,et al.  Phosphene induction by microstimulation of macaque V1 , 2007, Brain Research Reviews.

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

[24]  O. Blanke,et al.  Electrical Cortical Stimulation of the Human Prefrontal Cortex Evokes Complex Visual Hallucinations , 2000, Epilepsy & Behavior.

[25]  N. Logothetis,et al.  Visual competition , 2002, Nature Reviews Neuroscience.

[26]  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.

[27]  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.

[28]  Daniel Yoshor,et al.  Receptive fields in human visual cortex mapped with surface electrodes. , 2007, Cerebral cortex.