Linear transformation of thalamocortical input by intracortical excitation

Nature Neuroscience

Volumn 16, Issue 9, 2013, Pages 1324-1330

  Li, Ya Tang ^a   Ibrahim, Leena A ^a   Liu, Bao Hua ^a   Zhang, Li I ^a   Tao, Huizhong Whit ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MOUSE; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECEPTIVE FIELD; STRIATE CORTEX; THALAMOCORTICAL TRACT; VISUAL STIMULATION; VOLTAGE CLAMP;

ANIMALS; BRAIN MAPPING; CEREBRAL CORTEX; DEPENDOVIRUS; FEMALE; LINEAR MODELS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; NERVE NET; OPTOGENETICS; ORIENTATION; PARVALBUMINS; PHOTIC STIMULATION; RHODOPSIN; THALAMUS; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 84883415795     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3494     Document Type: Article

References (59)

1. Douglas, R.J. & Martin, K.A. A functional microcircuit for cat visual cortex. J. Physiol. (Lond.) 440, 735-769 (1991).
2. Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47-74 (1998).
3. 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).
4. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281-284 (1995).
5. 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).
6. Ferster, D. & Miller, K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441-471 (2000).
7. Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249-252 (1996).
8. 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).
9. Ben-Yishai, R., Bar-Or, R.L. & Sompolinsky, H. Theory of orientation tuning in visual cortex. Proc. Natl. Acad. Sci. USA 92, 3844-3848 (1995).
10. Somers, D.C., Nelson, S.B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448-5465 (1995).
11. Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A. & Suarez, H.H. Recurrent excitation in neocortical circuits. Science 269, 981-985 (1995).
12. Ben-Yishai, R., Hansel, D. & Sompolinsky, H. Traveling waves and the processing of weakly tuned inputs in a cortical network module. J. Comput. Neurosci. 4, 57-77 (1997).
13. Adorján, P., Levitt, J.B., Lund, J.S. & Obermayer, K. A model for the intracortical origin of orientation preference and tuning in macaque striate cortex. Vis. Neurosci. 16, 303-318 (1999).
14. McLaughlin, D., Shapley, R., Shelley, M. & Wielaard, D.J. A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4Calpha. Proc. Natl. Acad. Sci. USA 97, 8087-8092 (2000).
15. 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).
16. Khibnik, L.A., Cho, K.K. & Bear, M.F. Relative contribution of feedforward excitatory connections to expression of ocular dominance plasticity in layer 4 of visual cortex. Neuron 66, 493-500 (2010).
17. Yamauchi, T., Hori, T. & Takahashi, T. Presynaptic inhibition by muscimol through GABAB receptors. Eur. J. Neurosci. 12, 3433-3436 (2000).
18. Porter, J.T. & Nieves, D. Presynaptic GABAB receptors modulate thalamic excitation of inhibitory and excitatory neurons in the mouse barrel cortex. J. Neurophysiol. 92, 2762-2770 (2004).
19. Zhang, F., Aravanis, A.M., Adamantidis, A., de Lecea, L. & Deisseroth, K. Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 8, 577-581 (2007).
20. Bernstein, J.G., Garrity, P.A. & Boyden, E.S. Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits. Curr. Opin. Neurobiol. 22, 61-71 (2012).
21. 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).
22. Ma, W.P. et al. Visual representations by cortical somatostatin inhibitory neurons-selective, but with weak and delayed responses. J. Neurosci. 30, 14371-14379 (2010).
23. Liu, B.H. et al. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J. Neurosci. 29, 10520-10532 (2009).
24. Katzner, S. et al. Local origin of field potentials in visual cortex. Neuron 61, 35-41 (2009).
25. Pfrieger, F.W., Gottmann, K. & Lux, H.D. Kinetics of GABAB receptor-mediated inhibition of calcium currents and excitatory synaptic transmission in hippocampal neurons in vitro. Neuron 12, 97-107 (1994).
26. Niell, C.M. & Stryker, M.P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520-7536 (2008).
27. Priebe, N.J. & Ferster, D. Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57, 482-497 (2008).
28. Volgushev, M., Vidyasagar, T.R. & Pei, X. A linear model fails to predict orientation selectivity of cells in the cat visual cortex. J. Physiol. (Lond.) 496, 597-606 (1996).
29. Cruikshank, S.J., Urabe, H., Nurmikko, A.V. & Connors, B.W. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65, 230-245 (2010).
30. 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).
31. Bruno, R.M. & Sakmann, B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622-1627 (2006).
32. 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).
33. Kerlin, A.M., Andermann, M.L., Berezovskii, V.K. & Reid, R.C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67, 858-871 (2010).
34. Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87-91 (2011).
35. Liu, B.H. et al. Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71, 542-554 (2011).
36. Li, Y.T. et al. Broadening of inhibitory tuning underlies contrast-dependent sharpening of orientation selectivity in mouse visual cortex. J. Neurosci. 32, 16466-16477 (2012).
37. Atallah, B.V., Bruns, W., Carandini, M. & Scanziani, M. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73, 159-170 (2012).
38. Wilson, N.R., Runyan, C.A., Wang, F.L. & Sur, M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 343-348 (2012).
39. Lee, S.H. et al. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488, 379-383 (2012).
40. Liu, B.H. et al. Intervening inhibition underlies simple-cell receptive field structure in visual cortex. Nat. Neurosci. 13, 89-96 (2010).
41. Tan, A.Y., Brown, B.D., Scholl, B., Mohanty, D. & Priebe, N.J. Orientation selectivity of synaptic input to neurons in mouse and cat primary visual cortex. J. Neurosci. 31, 12339-12350 (2011).
42. Katzner, S., Busse, L. & Carandini, M. GABAA inhibition controls response gain in visual cortex. J. Neurosci. 31, 5931-5941 (2011).
43. Branco, T., Clark, B.A. & Hausser, M. Dendritic discrimination of temporal input sequences in cortical neurons. Science 329, 1671-1675 (2010).
44. Ohki, K., Chung, S., Ch'ng, Y.H., Kara, P. & Reid, R.C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597-603 (2005).
45. Allman, J., Miezin, F. & McGuinness, E. Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annu. Rev. Neurosci. 8, 407-430 (1985).
46. Gilbert, C.D. & Wiesel, T.N. The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Res. 30, 1689-1701 (1990).
47. Levitt, J.B. & Lund, J.S. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73-76 (1997).
48. Chisum, H.J., Mooser, F. & Fitzpatrick, D. Emergent properties of layer 2/3 neurons reflect the collinear arrangement of horizontal connections in tree shrew visual cortex. J. Neurosci. 23, 2947-2960 (2003).
49. Clopath, C., Busing, L., Vasilaki, E. & Gerstner, W. Connectivity reflects coding: a model of voltage-based STDP with homeostasis. Nat. Neurosci. 13, 344-352 (2010).
50. Ko, H. et al. The emergence of functional microcircuits in visual cortex. Nature 496, 96-100 (2013).
51. 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).
52. Lin, J.Y., Lin, M.Z., Steinbach, P. & Tsien, R.Y. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96, 1803-1814 (2009).
53. Li, Y.T., Ma, W.P., Pan, C.J., Zhang, L.I. & Tao, H.W. Broadening of cortical inhibition mediates developmental sharpening of orientation selectivity. J. Neurosci. 32, 3981-3991 (2012).
54. Wu, G.K., Li, P., Tao, H.W. & Zhang, L.I. Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron 52, 705-715 (2006).
55. Petreanu, L., Mao, T., Sternson, S.M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142-1145 (2009).
56. Zhang, M. et al. Functional elimination of excitatory feedforward inputs underlies developmental refinement of visual receptive fields in zebrafish. J. Neurosci. 31, 5460-5469 (2011).
57. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446 (2003).
58. Wu, G.K., Tao, H.W. & Zhang, L.I. From elementary synaptic circuits to information processing in primary auditory cortex. Neurosci. Biobehav. Rev. 35, 2094-2104 (2011).
59. Tan, A.Y., Zhang, L.I., Merzenich, M.M. & Schreiner, C.E. Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J. Neurophysiol. 92, 630-643 (2004).