Cortical neurons in thalamic recipient layers receive excitation from the thalamus and the cortex. The relative contribution of these two sources of excitation to sensory tuning is poorly understood. We optogenetically silenced the visual cortex of mice to isolate thalamic excitation onto layer 4 neurons during visual stimulation. Thalamic excitation contributed to a third of the total excitation and was organized in spatially offset, yet overlapping, ON and OFF receptive fields. This receptive field structure predicted the orientation tuning of thalamic excitation. Finally, both thalamic and total excitation were similarly tuned to orientation and direction and had the same temporal phase relationship to the visual stimulus. Our results indicate that tuning of thalamic excitation is unlikely to be imparted by direction- or orientation-selective thalamic neurons and that a principal role of cortical circuits is to amplify tuned thalamic excitation.
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Nelson, S., Toth, L., Sheth, B. & Sur, M. Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265, 774–777 (1994).
Anderson, J.S., Carandini, M. & Ferster, D. Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909–926 (2000).
Liu, B.H. et al. Intervening inhibition underlies simple-cell receptive field structure in visual cortex. Nat. Neurosci. 13, 89–96 (2010).
Liu, B.H. et al. Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71, 542–554 (2011).
Brecht, M. & Sakmann, B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J. Physiol. (Lond.) 543, 49–70 (2002).
Liu, B.H., Wu, G.K., Arbuckle, R., Tao, H.W. & Zhang, L.I. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat. Neurosci. 10, 1594–1600 (2007).
Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).
Chapman, B., Zahs, K.R. & Stryker, M.P. Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J. Neurosci. 11, 1347–1358 (1991).
Jin, J., Wang, Y., Swadlow, H.A. & Alonso, J.M. Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex. Nat. Neurosci. 14, 232–238 (2011).
Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).
Usrey, W.M., Alonso, J.M. & Reid, R.C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. J. Neurosci. 20, 5461–5467 (2000).
Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87–91 (2011).
Gilbert, C.D. & Wiesel, T.N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989).
Malach, R., Amir, Y., Harel, M. & Grinvald, A. Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proc. Natl. Acad. Sci. USA 90, 10469–10473 (1993).
Bosking, W.H., Zhang, Y., Schofield, B. & Fitzpatrick, D. Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J. Neurosci. 17, 2112–2127 (1997).
Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).
Olsen, S.R., Bortone, D.S., Adesnik, H. & Scanziani, M. Gain control by layer six in cortical circuits of vision. Nature 483, 47–52 (2012).
Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100, 13940–13945 (2003).
Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263–1268 (2005).
Atallah, B.V., Bruns, W., Carandini, M. & Scanziani, M. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73, 159–170 (2012).
Chung, S. & Ferster, D. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177–1189 (1998).
Piscopo, D.M., El-Danaf, R.N., Huberman, A.D. & Niell, C.M. Diverse visual features encoded in mouse lateral geniculate nucleus. J. Neurosci. 33, 4642–4656 (2013).
Grubb, M.S. & Thompson, I.D. Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. J. Neurophysiol. 90, 3594–3607 (2003).
Marshel, J.H., Kaye, A.P., Nauhaus, I. & Callaway, E.M. Anterior-posterior direction opponency in the superficial mouse lateral geniculate nucleus. Neuron 76, 713–720 (2012).
Lampl, I., Anderson, J.S., Gillespie, D.C. & Ferster, D. Prediction of orientation selectivity from receptive field architecture in simple cells of cat visual cortex. Neuron 30, 263–274 (2001).
Cudeiro, J. & Sillito, A.M. Looking back: corticothalamic feedback and early visual processing. Trends Neurosci. 29, 298–306 (2006).
Niell, C.M. & Stryker, M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479 (2010).
Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z.J. & Scanziani, M. A neural circuit for spatial summation in visual cortex. Nature 490, 226–231 (2012).
Haider, B., Häusser, M. & Carandini, M. Inhibition dominates sensory responses in the awake cortex. Nature 493, 97–100 (2013).
Lien, A.D. & Scanziani, M. In vivo labeling of constellations of functionally identified neurons for targeted in vitro recordings. Front. Neural Circuits 5, 16 (2011).
Briggman, K.L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188 (2011).
Bock, D.D. et al. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471, 177–182 (2011).
Jia, H., Rochefort, N.L., Chen, X. & Konnerth, A. Dendritic organization of sensory input to cortical neurons in vivo. Nature 464, 1307–1312 (2010).
Marshel, J.H., Mori, T., Nielsen, K.J. & Callaway, E.M. Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 67, 562–574 (2010).
Kitamura, K., Judkewitz, B., Kano, M., Denk, W. & Häusser, M. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat. Methods 5, 61–67 (2008).
Margrie, T.W., Brecht, M. & Sakmann, B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflügers Arch. 444, 491–498 (2002).
Brainard, D.H. The Psychophysics Toolbox. Spat. Vis. 10, 433–436 (1997).
Ringach, D.L., Shapley, R.M. & Hawken, M.J. Orientation selectivity in macaque V1: diversity and laminar dependence. J. Neurosci. 22, 5639–5651 (2002).
Swindale, N.V. Orientation tuning curves: empirical description and estimation of parameters. Biol. Cybern. 78, 45–56 (1998).
We thank J. Evora for help with genotyping and mouse husbandry, J. Isaacson, E. Chichilnisky and the members of the Scanziani and Isaacson laboratories for helpful discussions of this project, and S. Olsen and K. Reinhold for help with dLGN recordings. This project was supported by the Gatsby charitable foundation, the Brain and Behavior Research Foundation and the Howard Hughes Medical Institute.
The authors declare no competing financial interests.
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Lien, A., Scanziani, M. Tuned thalamic excitation is amplified by visual cortical circuits. Nat Neurosci 16, 1315–1323 (2013) doi:10.1038/nn.3488
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