Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex

THE function of the massive feedback projection from visual cortex to its thalamic relay nucleus1,2 has so far eluded any clear overview. This feedback exerts a range of effects3–6, including an increase in the inhibition elicited by moving contours7,8, but the functional logic of the direct connections to the thalamic cells that relay the retinal input to the cortex9–11 remains largely unknown. In contrast to its thalamic nucleus, the visual cortex is characterized by cells that are strongly sensitive to the orientation of moving contours. Here we report that when driven by moving oriented visual stimuli the cortical feedback induces correlated firing in relay cells. This cortically induced correlation of relay cell activity produces coherent firing in those groups of relay cells with receptive field alignments appropriate to signalling the particular orientation of the moving contour to the cortex. Synchronization of relay cell firing means that they will elicit temporally overlapping excitatory postsynaptic potentials in their cortical target cells, thus increasing the chance that the cortical cells will fire. Effectively this increases the gain of the input for feature-linked events detected by the cortex. We propose that this feedback loop serves to lock or focus the appropriate circuitry onto the stimulus feature.

[1]  W. Singer,et al.  Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry , 2004, Experimental Brain Research.

[2]  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.

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

[4]  R.T. Marrocco,et al.  Evidence for spatial structure in the cortical input to the monkey lateral geniculate nucleus , 2004, Experimental Brain Research.

[5]  K. Grant,et al.  Monosynaptic excitation of principal cells in the lateral geniculate nucleus by corticofugal fibers , 1982, Brain Research.

[6]  J. Robson The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat , 1983, The Journal of comparative neurology.

[7]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

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

[9]  R. Kalil,et al.  Synaptic connections between corticogeniculate axons and interneurons in the dorsal lateral geniculate nucleus of the cat , 1989, The Journal of comparative neurology.

[10]  M. Abeles Quantification, smoothing, and confidence limits for single-units' histograms , 1982, Journal of Neuroscience Methods.

[11]  P. C. Murphy,et al.  Corticofugal feedback influences the generation of length tuning in the visual pathway , 1987, Nature.

[12]  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.

[13]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

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