Functional response properties of VIP-expressing inhibitory neurons in mouse visual and auditory cortex

Frontiers in Neural Circuits

Volumn 9, Issue May, 2015, Pages

  Mesik, Lukas ^a,b   Ma, Wen Pei ^a   Li, Ling Yun ^a,b   Ibrahim, Leena A ^a,b   Huang, Z J ^c   Zhang, Li ^a,b   Tao, Huizhong W ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Direction selectivity; Frequency tuning; Intensityselectivity; Interneuron; Orientation selectivity; Receptive field property; Tonal receptive field; Visual receptive field

Indexed keywords

PARVALBUMIN; VASOACTIVE INTESTINAL POLYPEPTIDE; PHOTOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY SYSTEM FUNCTION; BRAIN FUNCTION; BRAIN REGION; CELL FUNCTION; CONTROLLED STUDY; EVOKED AUDITORY RESPONSE; EVOKED VISUAL RESPONSE; FEMALE; FUNCTIONAL ASSESSMENT; IMAGE ANALYSIS; LATENT PERIOD; MOLECULAR DYNAMICS; MOUSE; NEUROMODULATION; NONHUMAN; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; VISUAL CORTEX; VISUAL STIMULATION; VISUAL SYSTEM FUNCTION; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; MALE; METABOLISM; NERVE CELL INHIBITION; NONPARAMETRIC TEST; OPTOGENETICS; ORIENTATION; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOPHYSICS; REACTION TIME; TRANSGENIC MOUSE;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; FEMALE; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; OPTOGENETICS; ORIENTATION; PHOTIC STIMULATION; PSYCHOPHYSICS; REACTION TIME; STATISTICS, NONPARAMETRIC; VASOACTIVE INTESTINAL PEPTIDE; VISUAL CORTEX;

EID: 84935892967     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2015.00022     Document Type: Article

References (65)

1. Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z. J., and Scanziani, M. (2012). A neural circuit for spatial summation in visual cortex. Nature 490, 226-231. doi: 10.1038/nature11526
2. Alitto, H. J., and Dan, Y. (2012). Cell-type-specific modulation of neocortical activity by basal forebrain input. Front. Sys. Neurosci. 6:79. doi: 10.3389/fnsys.2012.00079
3. Arroyo, S., Bennett, C., Aziz, D., Brown, S. P., and Hestrin, S. (2012). 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. doi: 10.1523/JNEUR0SCI.0115-12.2012.
4. Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., Burkhalter, A., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi:10.1038/nrn2402
5. Atallah, B. V., Bruns, W., Carandini, M., and Scanziani, M. (2012). Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73, 159-170. doi: 10.1016/j.neuron.2011.12.013.
6. Carandini, M., and Heeger, D. J. (2011). Normalization as a canonical neural computation. Nat. Rev. Neurosci. 13, 51-62. doi: 10.1038/nrn3136.
7. Cauli, B., Porter, J. T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B., et al. (2000). Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc. Natl. Acad. Sci. U.S.A. 97, 6144-6149. doi: 10.1073/pnas.97.11.6144
8. Cauli, B., Tong, X. K., Rancillac, A., Serluca, N., Lambolez, B., Rossier, J., et al. (2004). Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940-8949. doi: 10.1523/JNEUR0SCI.3065-04.2004
9. Constantinople, C. M., and Bruno, R. M. (2011). Effects and mechanisms of wakefulness on local cortical networks. Neuron 69, 1061-1068. doi: 10.1016/j.neuron.2011.02.040
10. Dragoi, V., Sharma, J., and Sur, M. (2000). Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28, 287-298. doi: 10.1016/S0896-6273(00)00103-3
11. Ferezou, I., Cauli, B., Hill, E. L., Rossier, J., Hamel, E., and Lambolez, B. (2002). 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J. Neurosci. 22, 7389-7397.
12. Ferezou, I., Hill, E. L., Cauli, B., Gibelin, N., Kaneko, T., Rossier, J., et al. (2007). Extensive overlap of mu-opioid and nicotinic sensitivity in cortical interneurons. Cereb. Cortex 17, 1948-1957. doi: 10.1093/cercor/bhl104.
13. Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., et al. (2014). A cortical circuit for gain control by behavioral state. Cell 156, 1139-1152. doi:10.1016/j.cell.2014.01.050
14. Gentet, L. J., Kremer, Y., Taniguchi, H., Huang, Z. J., Staiger, J. F., and Petersen, C. C. (2012). Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612. doi: 10.1038/nn.3051.
15. Gonchar, Y., and Burkhalter, A. (1997). Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 74, 347-358. doi: 10.1093/cercor/7.4.347
16. Hirsch, J. A., Martinez, L. M., Pillai, C., Alonso, J. M., Wang, Q., and Sommer, F. T. (2003). Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat. Neurosci. 6, 1300-1308. doi: 10.1038/nn1152.
17. Hofer, S. B., Ko, H., Pichler, B., Vogelstein, J., Ros, H., Zeng, H., et al. (2011). Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat. Neurosci. 14, 1045-1052. doi: 10.1038/nn.2876
18. Isaacson, J. S., and Scanziani, M. (2011). How inhibition shapes cortical activity. Neuron 72,231-243.doi: 10.1016/j.neuron.2011.09.027
19. Ji, X. Y., Zingg, B., Mesik, L., Xiao, Z., Zhang, L. I., and Tao, H. W. (2015). Thalamocortical innervation pattern in mouse auditory and visual cortex: laminar andcell-type specificity. Cereb. Cortex. doi: 10.1093/cercor/bhv099
20. Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L., and Zhu, J. J. (2013). The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16, 210-218. doi: 10.1038/nn.3305
21. Kawaguchi, Y., and Kubota, Y. (1996). Physiological and morphological identification of somatostatin-or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J. Neurosci. 16, 2701-2715.
22. Kawaguchi, Y., and Kubota, Y. (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486. doi: 10.1093/cercor/7.6.476
23. Kerlin, A. M., Andermann, M. L., Berezovskii, V. K., and Reid, R. C. (2010). Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67, 858-871. doi: 10.1016/j.neuron.2010.08.002
24. Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J. Z., and Kepecs, A. (2013). Distinct behavioural and networkcorrelates of two interneuron types in prefrontal cortex. Nature 498, 363-366. doi: 10.1038/nature12176
25. Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G., and Rudy, B. (2010). The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30, 16796-16808. doi: 10.1523/JNEUR0SCI.1869-10.2010
26. Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G., and Rudy, B. (2013). A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16, 1662-1670. doi: 10.1038/nn.3544
27. Lee, S. H., Kwan, A. C., and Dan, Y. (2014). Interneuron subtypes and orientation tuning. Nature 508, E1-E2. doi: 10.1038/nature13128
28. Letzkus, J. J., Wolff, S. B., Meyer, E. M., Tovote, P., Courtin, J., Herry, C., et al. (2011).A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335. doi: 10.1038/nature10674.
29. Li, L. Y., Xiong, X. R., Ibrahim, L. A., Yuan, W., Tao, H. W., and Zhang, L. I. (2014a). Differential receptive field properties of parvalbumin and somatostatin inhibitory neurons in mouse auditory cortex. Cereb. Cortex 417. doi:10.1093/cercor/bht417[Epub ahead of print].
30. Li, L. Y., Ji, X. Y., Liang, F., Li, Y. T., Xiao, Z., Tao, H. W., et al. (2014b). A feedforward inhibitory circuit mediates lateral refinement of sensory representation in upper layer 2/3 of mouse primary auditory cortex. J. Neurosci. 34, 13670-13683. doi:10.1523/JNEUR0SCI.1516-14.2014.
31. Liu, B. H., Li, P., Li, Y. T., Sun, Y. J., Yanagawa, Y., Obata, K., et al. (2009). Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J. Neurosci. 29, 10520-10532. doi: 10.1523/JNEUR0SCI.1915-09.2009
32. Liu, B. H., Li, P., Sun, Y. J., Li, Y. T., Zhang, L. I., and Tao, H. W. (2010). Intervening inhibition underlies simple-cell receptive field structure in visual cortex. Nat. Neurosci. 13, 89-96. doi: 10.1038/nn.2443
33. Liu, B. H., Li, Y. T., Ma, W. P., Pan, C. J., Zhang, L. I., and Tao, H. W. (2011). Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71, 542-554. doi: 10.1016/j.neuron.2011.06.017.
34. Ma, W. P., Liu, B. H., Li, Y. T., Huang, Z. J., Zhang, L. I., and Tao, H. W. (2010). Visual representations by cortical somatostatin inhibitory neurons— selective but with weak and delayed responses. J. Neurosci. 30, 14371-14379. doi: 10.1523/JNEUR0SCI.3248-10.2010
35. Madisen, L., Mao, T., Koch, H., Zhuo, J. M., Berenyi, A., Fujisawa, S., et al. (2012).A toolbox of cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793-802. doi: 10.1038/nn.3078
36. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807. doi: 10.1038/nrn1519
37. Mata, M. L., and Ringach, D. L. (2005). Spatial overlap of ON and OFF subregions and its relation to response modulation ratio in macaque primary visual cortex. J. Neurophysiol. 93, 919-928. doi: 10.1152/jn.00668.2004
38. Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J., Battiste, J., et al. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582-1594. doi: 10.1523/JNEUR0SCI.4515-09.2010
39. Moore, A. K., and Wehr, M. (2013). Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J. Neurosci. 33, 13713-13723. doi: 10.1523/JNEUR0SCI.0663-13.2013
40. Nauhaus, I., Nielsen, K. J., and Callaway, E. M. (2012). Nonlinearity of two-photon Ca2+ imaging yields distorted measurements of tuning for V1 neuronal populations. J. Neurophysiol. 107, 923-936. doi: 10.1152/jn.00725.2011.
41. Niell, C. M., and Stryker, M. P. (2008). Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520-7536. doi: 10.1523/JNEUR0SCI.0623-08.2008.
42. Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., and Scanziani, M. (2013). Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068-1076. doi: 10.1038/nn.3446.
43. Pi, H. J., Hangya, B., Kvitsiani, D., Sanders, J. I., Huang, Z. J., and Kepecs, A. (2013). Cortical interneurons that specialize in disinhibitory control. Nature 503, 521-524. doi:10.1038/nature12676
44. Pologruto, T. A., Sabatini, B. L., and Svoboda, K. (2003). ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2:13. doi: 10.1186/1475-925X-2-13
45. Porter, J. T., Cauli, B., Tsuzuki, K., Lambolez, B., Rossier, J., and Audinat, E. (1999). Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J. Neurosci. 19, 5228-5235.
46. Rudy, B., Fishell, G., Lee, S., and Hjerling-Leffler, J. (2011). Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45-61. doi: 10.1002/dneu.20853
47. Runyan, C. A., Schummers, J., Van Wart, A., Kuhlman, S. J., Wilson, N. R., Huang, Z. J., et al. (2010). Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 67, 847-857. doi:10.1016/j.neuron.2010.08.006
48. Schumacher, J. W., Schneider, D. M., and Woolley, S. M. (2011). Anesthetic state modulates excitability but not spectral tuning or neural discrimination in single auditory midbrain neurons. J. Neurophysiol. 106, 500-514. doi: 10.1152/jn.01072.2010
49. Skottun, B. C., Grosof, D. H., and De Valois, R. L. (1991). 0n the responses of simple and complex cells to random dot patterns. Vision Res. 31, 43-46. doi: 10.1016/0042-6989(91)90071-C
50. Sun, Y. J., Kim, Y. J., Ibrahim, L. A., Tao, H. W., and Zhang, L. I. (2013). Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J. Neurosci. 33, 5326-5339. doi:10.1523/JNEUR0SCI.4810-12.2013
51. Sun, Y. J., Wu, G. K., Liu, B. H., Li, P., Zhou, M., Xiao, Z., et al. (2010). Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature 465, 927-931. doi: 10.1038/nature09079
52. Sutter, M. L., and Schreiner, C. E. (1991). Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J. Neurophysiol. 65, 1207-1226.
53. Tan, A. Y., Atencio, C. A., Polley, D. B., Merzenich, M. M., and Schreiner, C. E. (2007). Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons. Neuroscience 146, 449-462. doi: 10.1016/j.neuroscience.2007.01.019
54. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., et al. (2011). A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013. doi: 10.1016/j.neuron.2011.07.026
55. von Engelhardt, J., Eliava, M., Meyer, A. H., Rozov, A., and Monyer, H. (2007). Functional characterization of intrinsic cholinergic interneurons in the cortex. J. Neurosci. 27, 5633-5642. doi: 10.1523/JNEUR0SCI.4647-06.2007
56. Wang, Y., Gupta, A., Toledo-Rodriguez, M., Wu, C. Z., and Markram, H. (2002). Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb. Cortex 12, 395-410. doi:10.1093/cercor/12.4.395
57. Wilson, N. R., Runyan, C. A., Wang, F. L., and Sur, M. (2012). Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 343348. doi:10.1038/nature11347
58. Wu, G. K., Arbuckle, R., Liu, B. H., Tao, H. W., and Zhang, L. I. (2008). Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58, 132-143. doi: 10.1016/j.neuron.2008.01.035
59. Wu, G. K., Li, P., Tao, H. W., and Zhang, L. I. (2006). Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron 52, 705-715. doi: 10.1016/j.neuron.2006.10.009
60. Xiong, X. R., Liang, F., Li, H., Mesik, L., Zhang, K. K., Polley, D. B., et al. (2013). Interaural level difference-dependent gain control and synaptic scaling underlying binaural computation. Neuron 79, 738-753. doi: 10.1016/j.neuron.2013.06.012
61. Xu, X., and Callaway, E. M. (2009). Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J. Neurosci. 29, 70-85. doi: 10.1523/JNEUR0SCI.4104-08.2009
62. Xu, X., Roby, K. D., and Callaway, E. M. (2010). Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518, 389-404. doi: 10.1002/cne.22229
63. Zhang, L. I., Zhou, Y., and Tao, H. W. (2011). Perspectives on: information and coding in mammalian sensory physiology: inhibitory synaptic mechanisms underlying functional diversity in auditory cortex. J. Gen. Physiol. 138, 311-320. doi: 10.1085/jgp.201110650
64. Zhang, S., Xu, M., Kamigaki, T., Do, J. P. H., Chang, W. C., Jenvay, S., et al. (2014). Long-range and local circuits for top-down modulation ofvisual cortex processing. Science 345, 660-665. doi: 10.1126/science.1254126
65. Zhou, M., Tao, H. W., and Zhang, L. I. (2012). Generation of intensity selectivity by differential synaptic tuning: fast-saturating excitation but slow-saturating inhibition. J. Neurosci. 32, 18068-18078. doi: 10.1523/JNEUR0SCI.3647-12.2012