Oscillatory discharge in the visual system: does it have a functional role?

1. The discharge of individual neurons in the visual cortex and lateral geniculate nucleus (LGN) of anesthetized and paralyzed cats and kittens was examined for the presence of oscillatory activity. Neural firing was evoked through the monoptic or dichoptic presentation of drifting gratings and random sequences of flashed bars. The degree to which different oscillatory frequencies were present in neural discharge was quantified by computation of the power spectra of impulse train responses. 2. Action potentials from single cells were recorded extracellularly and isolated on the basis of amplitude. Receptive-field properties of the neurons under study were characterized initially by their discharge in response to gratings of sinusoidal luminance. By varying orientation and spatial frequency, optimal stimulus characteristics were determined. Oscillation analysis was performed on spike trains acquired during repeated presentations of the optimal stimulus by identification of power spectra peaks in the frequency range of rhythmic potentials observed in electroencephalograph studies (30-80 Hz). The amplitude and frequency of the largest peak in this range was used to characterize oscillatory strength and frequency. All discharge in which the peak amplitude exceeded the high-frequency noise by a factor > 1.5 was classified as oscillatory. 3. Of the 342 cortical cells examined, 147 cells displayed oscillatory activity in the 30 to 80-Hz range during portions of their visual response. Sixty out of 169 simple cells, 82 out of 166 complex cells, and 5 out of 7 special complex cells exhibited oscillations. There was no laminar bias in the distribution of oscillatory cells; the proportions of oscillatory cells were similar in all layers. All oscillatory discharge was variable with respect to frequency and strength between successive presentations of the same optimal stimulus. In as little as 10 s, for example, peak frequencies shifted by a factor of two. For many cells, these trial-to-trial variations obscured detectable oscillations when all trials were averaged together. 4. The potential role of neuronal maturation in the generation of oscillatory activity was investigated by studying neuronal responses from kittens at 4 wk postnatal. Of the 80 kitten cells studied, 27 exhibited oscillatory discharge. Although oscillations in the kitten visual cortex spanned the same frequency range as that seen in the adult, oscillations in the midfrequency range (36-44 Hz) are more common in the adult cortex. 5. To explore the possibility that oscillations might play a functional role in vision, we investigated the dependence of oscillations on different stimulus parameters.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[2]  D. Hubel,et al.  RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. , 1963, Journal of neurophysiology.

[3]  W. Levick,et al.  Statistical analysis of the dark discharge of lateral geniculate neurones , 1964, The Journal of physiology.

[4]  H. Barlow,et al.  Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit , 1964, The Journal of physiology.

[5]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

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

[7]  M. Verzeano,et al.  Periodic activity in the visual system of the cat. , 1967, Vision research.

[8]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[9]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

[10]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[11]  A. Harvey A physiological analysis of subcortical and commissural projections of areas 17 and 18 of the cat. , 1980, The Journal of physiology.

[12]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[13]  M. Ariel,et al.  Rhythmicity in rabbit retinal ganglion cell responses , 1983, Vision Research.

[14]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[15]  W. Freeman,et al.  Spatial EEG patterns, non-linear dynamics and perception: the neo-sherringtonian view , 1985, Brain Research Reviews.

[16]  I. Ohzawa,et al.  Contrast gain control in the cat's visual system. , 1985, Journal of neurophysiology.

[17]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  M. Stryker,et al.  Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  M. Cynader,et al.  The laminar distributions and postnatal development of neurotransmitter and neuromodulator receptors in cat visual cortex , 1986, Brain Research Bulletin.

[20]  I. Ohzawa,et al.  The binocular organization of complex cells in the cat's visual cortex. , 1986, Journal of neurophysiology.

[21]  The Fourier transform of a peristimulus time histogram can lead to erroneous results , 1986, Brain Research.

[22]  J. P. Jones,et al.  An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[23]  W. Freeman,et al.  Spatial patterns of visual cortical fast EEG during conditioned reflex in a rhesus monkey , 1987, Brain Research.

[24]  M. Dichter,et al.  Cellular mechanisms of epilepsy: a status report. , 1987, Science.

[25]  J. Robson,et al.  Nature of the maintained discharge of Q, X, and Y retinal ganglion cells of the cat. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[26]  T. Tsumoto,et al.  NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats , 1987, Nature.

[27]  Michael P. Stryker,et al.  Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin , 1988, Nature.

[28]  L. Maffei,et al.  Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. , 1988, Science.

[29]  G. Edelman,et al.  Reentrant signaling among simulated neuronal groups leads to coherency in their oscillatory activity. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[30]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[31]  M. Arndt,et al.  A neural network for feature linking via synchronous activity: Results from cat visual cortex and from simulations , 1989 .

[32]  J. Jacklet,et al.  Neuronal and cellular oscillators , 1989 .

[33]  J. Bouyer,et al.  Effect of DSP4, a neurotoxic agent, on attentive behaviour and related electrocortical activity in cat , 1989, Behavioural Brain Research.

[34]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[35]  P A Salin,et al.  Convergence and divergence in the afferent projections to cat area 17 , 1989, The Journal of comparative neurology.

[36]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[37]  W. Singer,et al.  The formation of cooperative cell assemblies in the visual cortex. , 1990, The Journal of experimental biology.

[38]  K I Naka,et al.  Dissection of the neuron network in the catfish inner retina. V. Interactions between NA and NB amacrine cells. , 1990, Journal of neurophysiology.

[39]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Receptive Field Properties and Feature Dependence , 1990, The European journal of neuroscience.

[40]  E Ahissar,et al.  Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. Koch,et al.  Some reflections on visual awareness. , 1990, Cold Spring Harbor symposia on quantitative biology.

[42]  H Sompolinsky,et al.  Global processing of visual stimuli in a neural network of coupled oscillators. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[43]  L. Maffei,et al.  Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[44]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Inter‐Columnar Interaction as Determined by Cross‐Correlation Analysis , 1990, The European journal of neuroscience.

[45]  J. Bolz,et al.  Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlation study , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  D. Baylor,et al.  Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. , 1991, Science.

[47]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[48]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[49]  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10-to 50-Hz frequency range , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[50]  A model for cortical 40 Hz oscillations invokes inter-area interactions. , 1991, Neuroreport.

[51]  D. Paré,et al.  Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[52]  R. Llinás,et al.  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Stephen Grossberg,et al.  Synchronized oscillations during cooperative feature linking in a cortical model of visual perception , 1991, Neural Networks.

[54]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[55]  W. Singer,et al.  Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties , 1992, Visual Neuroscience.

[56]  W. Singer,et al.  Mechanisms Underlying the Generation of Neuronal Oscillations in Cat Visual Cortex , 1992 .