Long-range traveling waves of activity triggered by local dichoptic stimulation in V1 of behaving monkeys.

Traveling waves of cortical activity, in which local stimulation triggers lateral spread of activity to distal locations, have been hypothesized to play an important role in cortical function. However, there is conflicting physiological evidence for the existence of spreading traveling waves of neural activity triggered locally. Dichoptic stimulation, in which the two eyes view dissimilar monocular patterns, can lead to dynamic wave-like fluctuations in visual perception and therefore, provides a promising means for identifying and studying cortical traveling waves. Here, we used voltage-sensitive dye imaging to test for the existence of traveling waves of activity in the primary visual cortex of awake, fixating monkeys viewing dichoptic stimuli. We find clear traveling waves that are initiated by brief, localized contrast increments in one of the monocular patterns and then, propagate at speeds of ∼ 30 mm/s. These results demonstrate that under an appropriate visual context, circuitry in visual cortex in alert animals is capable of supporting long-range traveling waves triggered by local stimulation.

[1]  Amiram Grinvald,et al.  VSDI: a new era in functional imaging of cortical dynamics , 2004, Nature Reviews Neuroscience.

[2]  Eyal Seidemann,et al.  Uniform spatial spread of population activity in primate parafoveal V1. , 2012, Journal of neurophysiology.

[3]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[4]  Randolph Blake,et al.  Hierarchy of cortical responses underlying binocular rivalry , 2007, Nature Neuroscience.

[5]  F. Chavane,et al.  Dynamics of Local Input Normalization Result from Balanced Short- and Long-Range Intracortical Interactions in Area V1 , 2012, The Journal of Neuroscience.

[6]  James T. Mcllwain Point images in the visual system: new interest in an old idea , 1986, Trends in Neurosciences.

[7]  E. Seidemann,et al.  Optimal temporal decoding of neural population responses in a reaction-time visual detection task. , 2008, Journal of neurophysiology.

[8]  Alan W Freeman,et al.  Multistage model for binocular rivalry. , 2005, Journal of neurophysiology.

[9]  Tatsuo K Sato,et al.  Traveling Waves in Visual Cortex , 2012, Neuron.

[10]  Amiram Grinvald,et al.  Imaging Cortical Dynamics at High Neurotechnique Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999 .

[11]  E. Seidemann,et al.  Optimal decoding of correlated neural population responses in the primate visual cortex , 2006, Nature Neuroscience.

[12]  Dov Sagi,et al.  Opposite Neural Signatures of Motion-Induced Blindness in Human Dorsal and Ventral Visual Cortex , 2008, The Journal of Neuroscience.

[13]  Yevgeniy B. Sirotin,et al.  The neuroimaging signal is a linear sum of neurally distinct stimulus- and task-related components , 2012, Nature Neuroscience.

[14]  Robert A. Frazor,et al.  Standing Waves and Traveling Waves Distinguish Two Circuits in Visual Cortex , 2007, Neuron.

[15]  Eyal Seidemann,et al.  The relationship between voltage-sensitive dye imaging signals and spiking activity of neural populations in primate V1. , 2012, Journal of neurophysiology.

[16]  D. Heeger,et al.  Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry , 2000, Nature Neuroscience.

[17]  Stephen A. Engel,et al.  Interocular rivalry revealed in the human cortical blind-spot representation , 2001, Nature.

[18]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[19]  R. Fox,et al.  Effect of binocular rivalry suppression on the motion aftereffect , 1975, Vision Research.

[20]  David J Heeger,et al.  Rapid and precise retinotopic mapping of the visual cortex obtained by voltage-sensitive dye imaging in the behaving monkey. , 2007, Journal of neurophysiology.

[21]  D. Heeger,et al.  In this issue , 2002, Nature Reviews Drug Discovery.

[22]  Sabine Kastner,et al.  Neural correlates of binocular rivalry in the human lateral geniculate nucleus , 2005, Nature Neuroscience.

[23]  R. Blake,et al.  Neural bases of binocular rivalry , 2006, Trends in Cognitive Sciences.

[24]  M. Lauritzen Reading vascular changes in brain imaging: is dendritic calcium the key? , 2005, Nature Reviews Neuroscience.

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

[26]  Timothy J. Andrews,et al.  Form and motion have independent access to consciousness , 1999, Nature Neuroscience.

[27]  N. Wade,et al.  The influence of colour and contour rivalry on the magnitude of the tilt after-effect , 1978, Vision Research.

[28]  N. Logothetis,et al.  Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry , 1996, Nature.

[29]  Y. Hayashi,et al.  The visual field representation of the rat ventral lateral geniculate nucleus , 1984, The Journal of comparative neurology.

[30]  F. Chavane,et al.  Imaging cortical correlates of illusion in early visual cortex , 2004, Nature.

[31]  Yevgeniy B. Sirotin,et al.  Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity. , 2009, Nature.

[32]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  R. P. O'Shea,et al.  Interocular transfer of the motion after-effect is not reduced by binocular rivalry , 1981, Vision Research.

[34]  H. Wilson,et al.  Dynamics of travelling waves in visual perception , 2001, Nature.

[35]  E. Seidemann,et al.  Complex Dynamics of V1 Population Responses Explained by a Simple Gain-Control Model , 2009, Neuron.

[36]  Hugh R Wilson,et al.  Computational evidence for a rivalry hierarchy in vision , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  D. G. Albrecht,et al.  Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? , 2000, Nature Neuroscience.

[38]  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.

[39]  Georgios A. Keliris,et al.  The Role of the Primary Visual Cortex in Perceptual Suppression of Salient Visual Stimuli , 2010, The Journal of Neuroscience.

[40]  Andreas Bartels,et al.  fMRI and its interpretations: an illustration on directional selectivity in area V5/MT , 2008, Trends in Neurosciences.

[41]  C. Clifford,et al.  Suppressed Patterns Alter Vision during Binocular Rivalry , 2005, Current Biology.

[42]  Jeremy M. Wolfe,et al.  Reversing ocular dominance and suppression in a single flash , 1984, Vision Research.

[43]  Randolph Blake,et al.  Traveling waves of activity in primary visual cortex during binocular rivalry , 2005, Nature Neuroscience.

[44]  Randolph Blake,et al.  Strength of early visual adaptation depends on visual awareness. , 2010, Proceedings of the National Academy of Sciences of the United States of America.