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Thalamic interneurons and relay cells use complementary synaptic mechanisms for visual processing

Abstract

Synapses made by local interneurons dominate the thalamic circuits that process signals traveling from the eye downstream. The anatomical and physiological differences between interneurons and the (relay) cells that project to cortex are vast. To explore how these differences might influence visual processing, we made intracellular recordings from both classes of cells in vivo in cats. Macroscopically, all receptive fields were similar, consisting of two concentrically arranged subregions in which dark and bright stimuli elicited responses of the reverse sign. Microscopically, however, the responses of the two types of cells had opposite profiles. Excitatory stimuli drove trains of single excitatory postsynaptic potentials in relay cells, but graded depolarizations in interneurons. Conversely, suppressive stimuli evoked smooth hyperpolarizations in relay cells and unitary inhibitory postsynaptic potentials in interneurons. Computational analyses suggested that these complementary patterns of response help to preserve information encoded in the fine timing of retinal spikes and to increase the amount of information transmitted to cortex.

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Figure 1: Push-pull responses of an OFF-center relay cell and ON-center interneuron.
Figure 2: Receptive fields of relay cells and interneurons and prediction of neural responses using linear-nonlinear models.
Figure 3: Quantitative comparison of postsynaptic currents recorded from all cells.
Figure 4: Voltage dependence of postsynaptic potentials recorded from relay cells and interneurons.
Figure 5: Visual modulation of synaptic inputs to relay cells and interneurons.
Figure 6: Rates of unitary synaptic events recorded from relay cells and interneurons.
Figure 7: Spatial distribution of relay cells and interneurons.
Figure 8: Simulations of information transmitted by circuits that use different forms of synaptic integration.

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Acknowledgements

We are grateful to L.M. Martinez for discussions throughout the project and thank Q. Wang for custom software. J. Provost, S.X.X. Xing, B. Gary, M. Bathen and M. Gerstmar reconstructed labeled cells, and M. Gerstmar also assisted with event sorting. This work was supported by the US National Institutes of Health (EY09593, J.A.H.), the Redwood Center for Theoretical Neuroscience (F.T.S.) and the National Science Foundation (IIS-0713657, F.T.S.).

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X.W. and J.A.H. performed the experiments with help from V.V. and C.S.S. X.W., J.A.H. and F.T.S. contributed to various analyses, and X.W. and F.T.S. developed the simulations. X.W., J.A.H. and F.T.S. wrote the manuscript, and X.W. prepared all of the figures.

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Correspondence to Judith A Hirsch.

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Wang, X., Vaingankar, V., Soto Sanchez, C. et al. Thalamic interneurons and relay cells use complementary synaptic mechanisms for visual processing. Nat Neurosci 14, 224–231 (2011). https://doi.org/10.1038/nn.2707

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