Microstimulation Reveals Limits in Detecting Different Signals from a Local Cortical Region

Behavioral performance depends on the activity of neurons in sensory cortex, but little is known about the brain's capacity to access specific neuronal signals to guide behavior. Even the individual sensory neurons that are most sensitive to a relevant stimulus are only weakly correlated with behavior, suggesting that behavioral decisions are based on the combined activity of groups of neurons with sensitivities well matched to task demands. To explore how flexibly different patterns of activity can be accessed from a given cortical region, we trained animals to detect electrical microstimulation of local V1 sites. By allowing the animals to become expert at the detection of microstimulation of specific V1 sites that corresponded to particular retinotopic locations, we could measure the effects of that training on the ability of those sites to support the detection of visual stimuli. Training to detect electrical activation caused a large, reversible, retinotopically localized impairment of thresholds for detecting visual stimuli. Retraining on visual detection restored normal thresholds and in turn impaired thresholds for detecting microstimulation. These results suggest that there are substantial limits to the types of signals for which a local cortical region can be simultaneously optimized.

[1]  R.N.Dej.,et al.  The Cerebral Cortex of Man , 1951, Neurology.

[2]  Daniel Yoshor,et al.  Perceiving Electrical Stimulation of Identified Human Visual Areas , 2009, NeuroImage.

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

[4]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[5]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Misha Tsodyks,et al.  Neural networks and perceptual learning , 2004, Nature.

[7]  R. Doty,et al.  Laminar variation in threshold for detection of electrical excitation of striate cortex by macaques. , 2005, Journal of neurophysiology.

[8]  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.

[9]  Jeffrey D. Schall,et al.  Neural basis of deciding, choosing and acting , 2001, Nature Reviews Neuroscience.

[10]  C. Gilbert,et al.  Learning to find a shape , 2000, Nature Neuroscience.

[11]  Warren M Slocum,et al.  What delay fields tell us about striate cortex. , 2007, Journal of neurophysiology.

[12]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[14]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[15]  Steven R. Holloway,et al.  Seeing what is not there shows the costs of perceptual learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[17]  G. DeAngelis,et al.  Fine Discrimination Training Alters the Causal Contribution of Macaque Area MT to Depth Perception , 2008, Neuron.

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

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

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

[21]  C. Law,et al.  Reinforcement learning can account for associative and perceptual learning on a visual decision task , 2009, Nature Neuroscience.

[22]  E. J. Tehovnik,et al.  Phosphene induction and the generation of saccadic eye movements by striate cortex. , 2005, Journal of neurophysiology.

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

[24]  D. Scott Perceptual learning. , 1974, Queen's nursing journal.

[25]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[26]  M. Mladejovsky,et al.  Artificial Vision for the Blind: Electrical Stimulation of Visual Cortex Offers Hope for a Functional Prosthesis , 1974, Science.

[27]  Matthias M. Müller,et al.  Changed perceptions in Braille readers , 1998, Nature.

[28]  W. Merigan,et al.  Motion perception following lesions of the superior temporal sulcus in the monkey. , 1994, Cerebral cortex.