Visual stimuli modulate precise synchronous firing within the thalamus.

The work of Mircea Steriade demonstrated that the neocortex could synchronize large regions of the thalamus within 10-100 milliseconds (for review see Steriade and Timofeev, 2003, Steriade, 2005). Unlike the synchrony generated by the cortex, the retinal afferents synchronize a restricted group of neighboring thalamic neurons with <1-millisecond precision (Alonso et al., 1996, Yeh et al., 2003). Here, we use a large sample (n= 372) of simultaneous recordings from neighboring neurons in the Lateral Geniculate Nucleus (LGN) to illustrate the high specificity of the synchrony generated by retinal afferents and its dependency on sensory stimulation. First, we demonstrate that cells sharing a retinal afferent show a balanced receptive field diversity: while slight receptive field mismatches are common, the largest mismatches in a specific property (e.g. receptive field size) are restricted to cells that are precisely matched in other properties (e.g. receptive field overlap). Second, we show that these receptive field mismatches are functionally important and can lead to a 5-fold variation in the percentage of synchronous spikes driven by the shared retinal afferent under different stimulus conditions. Based on these and other findings, we speculate that the precise synchronous firing of cells sharing a retinal afferent could serve to amplify local stimuli that may be too brief and small to generate a large number of thalamic spikes.

[1]  R. Shapley,et al.  The use of m-sequences in the analysis of visual neurons: Linear receptive field properties , 1997, Visual Neuroscience.

[2]  J. Alonso,et al.  Retinogeniculate connections: A balancing act between connection specificity and receptive field diversity. , 2006, Progress in brain research.

[3]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

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

[5]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[6]  S. Sherman,et al.  Synaptic circuits involving an individual retinogeniculate axon in the cat , 1987, The Journal of comparative neurology.

[7]  M. Castro-Alamancos Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo , 2002, The Journal of physiology.

[8]  Luis M Martinez,et al.  Synaptic physiology of the flow of information in the cat's visual cortex in vivo , 2002, The Journal of physiology.

[9]  D. Mastronarde Correlated firing of retinal ganglion cells , 1989, Trends in Neurosciences.

[10]  F. Mechler,et al.  Independent and Redundant Information in Nearby Cortical Neurons , 2001, Science.

[11]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[12]  G. Orban,et al.  Velocity selectivity in the cat visual system. I. Responses of LGN cells to moving bar stimuli: a comparison with cortical areas 17 and 18. , 1985, Journal of neurophysiology.

[13]  D N Mastronarde,et al.  Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: Receptive-field properties and retinal inputs , 1992, Visual Neuroscience.

[14]  B. B. Lee,et al.  A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. , 1985, The Journal of physiology.

[15]  R C Reid,et al.  Efficient Coding of Natural Scenes in the Lateral Geniculate Nucleus: Experimental Test of a Computational Theory , 1996, The Journal of Neuroscience.

[16]  M. Schnitzer,et al.  Multineuronal Firing Patterns in the Signal from Eye to Brain , 2003, Neuron.

[17]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[18]  J. Alonso,et al.  Two different types of Y cells in the cat lateral geniculate nucleus. , 2003, Journal of neurophysiology.

[19]  Reid R. Clay,et al.  Specificity and strength of retinogeniculate connections. , 1999, Journal of neurophysiology.

[20]  H. Swadlow,et al.  The impact of 'bursting' thalamic impulses at a neocortical synapse , 2001, Nature Neuroscience.

[21]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. , 1987, Journal of neurophysiology.

[22]  D. Ferster,et al.  Prediction of Orientation Selectivity from Receptive Field Architecture in Simple Cells of Cat Visual Cortex , 2001, Neuron.

[23]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[24]  R. Eckhorn,et al.  A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors , 1993, Journal of Neuroscience Methods.

[25]  G L Gerstein,et al.  Detecting spatiotemporal firing patterns among simultaneously recorded single neurons. , 1988, Journal of neurophysiology.

[26]  S. Nelson,et al.  Short-Term Depression at Thalamocortical Synapses Contributes to Rapid Adaptation of Cortical Sensory Responses In Vivo , 2002, Neuron.

[27]  C. Brody Slow covariations in neuronal resting potentials can lead to artefactually fast cross-correlations in their spike trains. , 1998, Journal of neurophysiology.

[28]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[29]  W. Levick,et al.  Simultaneous recording of input and output of lateral geniculate neurones. , 1971, Nature: New biology.

[30]  C. Gray The Temporal Correlation Hypothesis of Visual Feature Integration Still Alive and Well , 1999, Neuron.

[31]  B. Sakmann,et al.  Cortex Is Driven by Weak but Synchronously Active Thalamocortical Synapses , 2006, Science.

[32]  R. Reid,et al.  Precisely correlated firing in cells of the lateral geniculate nucleus , 1996, Nature.

[33]  B. B. Lee,et al.  The retinal input to cells in area 17 of the cat's cortex , 1977, Experimental Brain Research.

[34]  S. Hecht,et al.  ENERGY, QUANTA, AND VISION , 1942, The Journal of general physiology.

[35]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[36]  W. Regehr,et al.  Developmental Remodeling of the Retinogeniculate Synapse , 2000, Neuron.

[37]  Ee Sutter,et al.  A deterministic approach to nonlinear systems analysis , 1992 .

[38]  R. Reid,et al.  Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus , 1998, Nature.

[39]  Dario L Ringach,et al.  Haphazard wiring of simple receptive fields and orientation columns in visual cortex. , 2004, Journal of neurophysiology.

[40]  Jose-Manuel Alonso,et al.  Neurons Find Strength Through Synchrony in the Brain , 2006, Science.

[41]  M. Steriade Sleep, epilepsy and thalamic reticular inhibitory neurons , 2005, Trends in Neurosciences.

[42]  M. Steriade,et al.  Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations , 2003, Neuron.

[43]  Iman H. Brivanlou,et al.  Mechanisms of Concerted Firing among Retinal Ganglion Cells , 1998, Neuron.