Response-dependent dynamics of cell-specific inhibition in cortical networks in vivo

Nature Communications

Volumn 5, Issue , 2014, Pages

  El Boustani, Sami ^a   Sur, Mriganka ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; SOMATOSTATIN; BIOLOGICAL MARKER; FLUORESCENT DYE;

CELL ORGANELLE; GENE EXPRESSION; IMMUNE RESPONSE; INHIBITION; NEUROLOGY; PHYSIOLOGICAL RESPONSE;

ADULT; ANIMAL CELL; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; FEMALE; IN VIVO STUDY; LATENT PERIOD; MALE; MOLECULAR DYNAMICS; MOLECULAR PROBE; MOUSE; NERVE CELL INHIBITION; NONHUMAN; OPTOGENETICS; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RECEPTIVE FIELD; SENSORY SYSTEM ELECTROPHYSIOLOGY; STRIATE CORTEX; TARGET CELL; VISUAL STIMULATION; ACTION POTENTIAL; ANIMAL; CLASSIFICATION; CYTOLOGY; ELECTRODE IMPLANT; GENE EXPRESSION; METABOLISM; NERVE CELL; PHOTOSTIMULATION; PHYSIOLOGY; STEREOTACTIC PROCEDURE; TIME; TRANSGENIC MOUSE; VISUAL CORTEX; VISUAL SYSTEM;

MUS;

ACTION POTENTIALS; ANIMALS; BIOMARKERS; ELECTRODES, IMPLANTED; FLUORESCENT DYES; GENE EXPRESSION; MICE; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; OPTOGENETICS; PARVALBUMINS; PHOTIC STIMULATION; SOMATOSTATIN; STEREOTAXIC TECHNIQUES; TIME FACTORS; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84923351932     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6689     Document Type: Article

References (56)

1. Silver, R. A. Neuronal arithmetic. Nat. Rev. Neurosci. 11, 474-489 (2010
2. Haider, B. & McCormick, D. A. Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62, 171-189 (2009
3. Carandini, M. & Heeger, D. Normalization as a canonical neural computation. Nat. Rev. Neurosci. 13, 51-62 (2012
4. Katzner, S., Busse, L. & Carandini, M. GABAA inhibition controls response gain in visual cortex. J. Neurosci. 31, 5931-5941 (2011
5. Salinas, E. & Thier, P. Gain modulation: a major computational principle of the central nervous system. Neuron 27, 15-21 (2000
6. McAdams, C. J. & Maunsell, J. H. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431-441 (1999
7. Treue, S. & Martńez Trujillo, J. C. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575-579 (1999
8. Reynolds, J. H. & Heeger, D. J. The normalization model of attention. Neuron 61, 168-185 (2009
9. Somers, D., Nelson, S. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 75, 5448-5465 (1995
10. Anderson, J. S. The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290, 1968-1972 (2000
11. Ohshiro, T., Angelaki, D. E. & DeAngelis, G. C. A normalization model of multisensory integration. Nat. Neurosci. 14, 775-782 (2011
12. Louie, K. & Glimcher, P. W. Separating value from choice: delay discounting activity in the lateral intraparietal area. J. Neurosci. 30, 5498-5507 (2010
13. 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
14. Wilson, N. R., Runyan, C. a., Wang, F. L. & Sur, M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 1-6 (2012
15. Lee, S.-H. et al. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488, 379-383 (2012
16. Doiron, B., Longtin, A., Berman, N. & Maler, L. Subtractive and divisive inhibition: effect of voltage-dependent inhibitory conductances and noise. Neural Comput. 13, 227-248 (2001
17. Holt, G. R. & Koch, C. Shunting inhibition does not have a divisive effect on firing rates. Neural Comput. 9, 1001-1013 (1997
18. Mitchell, S. J. & Silver, R. A. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445 (2003
19. Murphy, B. K. & Miller, K. D. Multiplicative gain changes are induced by excitation or inhibition alone. J. Neurosci. 23, 10040-10051 (2003
20. Ascoli, G. a. et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568 (2008
21. Markram, H. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807 (2004
22. Moore, C. I., Carlen, M., Knoblich, U. & Cardin, J. a. Neocortical interneurons: from diversity, strength. Cell 142, 189-193 (2010
23. Petersen, C. C. H. & Crochet, S. Synaptic computation and sensory processing in neocortical layer 2/3. Neuron 78, 28-48 (2013
24. Alitto, H. J. & Dan, Y. Function of inhibition in visual cortical processing. Curr. Opin. Neurobiol. 20, 340-346 (2010
25. Pfeffer, C. K., Xue, M., He, M., Huang, Z. J. & Scanziani, M. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068-1076 (2013
26. Atallah, B., Bruns, W., Carandini, M. & Scanziani, M. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73, 159-170 (2012
27. Lee, S.-H., Kwan, A. C. & Dan, Y. Interneuron subtypes and orientation tuning. Nature 508, E1-E2 (2014
28. El-Boustani, S., Wilson, N. R., Runyan, C. a. & Sur, M. El-Boustani et al. reply. Nature 508, E3-E4 (2014
29. Kulik, A. et al. Compartment-dependent colocalization of Kir3.2-containing K+ channels and GABAB receptors in hippocampal pyramidal cells. J. Neurosci. 26, 4289-4297 (2006
30. Nusser, Z., Sieghart, W., Benke, D., Fritschy, J. M. & Somogyi, P. Differential synaptic localization of two major gamma-Aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc. Natl Acad. Sci. USA 93, 11939-11944 (1996
31. Chance, F. S., Abbott, L. F. & Reyes, A. D. Gain modulation from background synaptic input. Neuron 35, 773-782 (2002
32. Abbott, L. F. & Chance, F. S. Drivers and modulators from push-pull and balanced synaptic input. Prog. Brain Res. 149, 147-155 (2005
33. Ma, W. et al. Visual representations by cortical somatostatin inhibitory neurons-selective but with weak and delayed responses. J. Neurosci. 30, 14371-14379 (2010
34. 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
35. Liu, B. et al. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J. Neurosci. 29, 10520-10532 (2009
36. Vogelstein, J. T. et al. Fast nonnegative deconvolution for spike train inference from population calcium imaging. J. Neurophysiol. 104, 3691-3704 (2010
37. Yeh, C.-I., Xing, D., Williams, P. E. & Shapley, R. M. Stimulus ensemble and cortical layer determine V1 spatial receptive fields. Proc. Natl Acad. Sci. USA 106, 14652-14657 (2009
38. Bonin, V., Histed, M. H., Yurgenson, S. & Reid, R. C. Local diversity and finescale organization of receptive fields in mouse visual cortex. J. Neurosci. 31, 18506-18521 (2011
39. Xu, H., Jeong, H.-Y., Tremblay, R. & Rudy, B. Neocortical somatostatinexpressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77, 155-167 (2013
40. Cottam, J. C. H., Smith, S. L. & Häusser, M. Target-specific effects of somatostatin-expressing interneurons on neocortical visual processing. J. Neurosci. 33, 19567-19578 (2013
41. Cardin, J. a. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667 (2009
42. Haider, B., Häusser, M. & Carandini, M. Inhibition dominates sensory responses in the awake cortex. Nature 493, 97-100 (2013
43. Polack, P.-O., Friedman, J. & Golshani, P. Cellular mechanisms of brain statedependent gain modulation in visual cortex. Nat. Neurosci. 16, 1331-1339 (2013
44. Pi, H.-J. et al. Cortical interneurons that specialize in disinhibitory control. Nature 503, 521-524 (2013
45. Fu, Y. et al. A cortical circuit for gain control by behavioral state. Cell 156, 1139-1152 (2014
46. Yger, P., El Boustani, S., Destexhe, A. & Frégnac, Y. Topologically invariant macroscopic statistics in balanced networks of conductance-based integrateand-fire neurons. J. Comput. Neurosci. 31, 229-245 (2011
47. Softky, W. R. & Koch, C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13, 334-350 (1993
48. Herman, A. M., Huang, L., Murphey, D. K., Garcia, I. & Arenkiel, B. R. Cell type-specific and time-dependent light exposure contribute to silencing in neurons expressing Channelrhodopsin-2. Elife 3, e01481-e01481 (2014
49. Atallah, B. V., Scanziani, M. & Carandini, M. Atallah et al. reply. Nature 508, E3 (2014
50. Arroyo, S., Bennett, C., Aziz, D., Brown, S. P. & Hestrin, S. Prolonged disynaptic inhibition in the cortex mediated by slow, non-A7 nicotinic excitation of a specific subset of cortical interneurons. J. Neurosci. 32, 3859-3864 (2012
51. Gentet, L. J. et al. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 1-7 (2012
52. Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013
53. Vogels, T. P. & Abbott, L. F. Signal propagation and logic gating in networks of integrate-And-fire neurons. J. Neurosci. 25, 10786-10795 (2005
54. Kumar, A., Schrader, S., Aertsen, A. & Rotter, S. The high-conductance state of cortical networks. Neural Comput. 20, 1-43 (2008
55. Diesmann, M. & Gewaltig, M.-O. in Forschung und wisschenschaftliches Rechnen, Beiträge zum Heinz-Billing-Preis 2001 Vol. 58 (eds Plesser, T. & Macho, V.) 43-70 (2002
56. Davison, A. P. et al. PyNN: a common interface for neuronal network simulators. Front. Neuroinform. 2, 11 (2008).