From circuit motifs to computations: Mapping the behavioral repertoire of cortical interneurons

Current Opinion in Neurobiology

Volumn 26, Issue , 2014, Pages 117-124

  Hangya, Balázs ^a,b   Pi, Hyun Jae ^a   Kvitsiani, Duda ^a   Ranade, Sachin P ^a   Kepecs, Adam ^a  

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

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; SOMATOSTATIN;

ANTERIOR CINGULATE; BRAIN MAPPING; CELL ACTIVITY; CELL FUNCTION; DENDRITE; GENE TARGETING; GLIA CELL; HIPPOCAMPUS; INTERNEURON; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PYRAMIDAL NERVE CELL; REFRACTORY PERIOD; REVIEW; SENSORY CORTEX; SYNAPTIC TRANSMISSION; VISUAL CORTEX; ANIMAL; BEHAVIOR; BIOLOGICAL MODEL; BRAIN CORTEX; CYTOLOGY; NERVE CELL NETWORK; PHYSIOLOGY;

ANIMALS; BEHAVIOR; BRAIN MAPPING; CEREBRAL CORTEX; INTERNEURONS; MODELS, NEUROLOGICAL; NERVE NET;

EID: 84893490346     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.01.007     Document Type: Review

References (88)

1. Cajal SR: Recollections of My Life [E.H. Craigie and J. Cano, Trans.] MIT Press; 1989 [1937].
2. Douglas R.J., Martin K.A. Mapping the matrix: the ways of neocortex. Neuron 2007, 56:226-238.
3. Mountcastle V.B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 1957, 20:408-434.
4. Hubel D.H., Wiesel T.N. Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol 1972, 146:421-450.
5. Szentagothai J. The neuron network of the cerebral cortex: a functional interpretation. Proc R Soc Lond B Biol Sci 1977, 201:219-248.
6. Azouz R., Gray C.M., Nowak L.G., McCormick D.A. Physiological properties of inhibitory interneurons in cat striate cortex. Cereb Cortex 1997, 7:534-545.
7. Csicsvari J., Hirase H., Czurko A., Buzsaki G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 1998, 21:179-189.
8. Kvitsiani D., Ranade S., Hangya B., Taniguchi H., Huang J.Z., Kepecs A. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 2013, 498:363-366.
9. Wilent W.B., Nitz D.A. Discrete place fields of hippocampal formation interneurons. J Neurophysiol 2007, 97:4152-4161.
10. Ego-Stengel V., Wilson M.A. Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus 2007, 174:161-174.
11. Kubie J.L., Muller R.U., Bostock E. Spatial firing properties of hippocampal theta cells. J Neurosci 1990, 10:1110-1123.
12. Marshall L., Henze D.A., Hirase H., Leinekugel X., Dragoi G., Buzsaki G. Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge. J Neurosci 2002, 22:RC197.
13. Maurer A.P., Cowen S.L., Burke S.N., Barnes C.A., McNaughton B.L. Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. J Neurosci 2006, 26:13485-13492.
14. Hangya B., Li Y., Muller R.U., Czurkó A. Complementary spatial firing in place cell-interneuron pairs. J Physiol 2010, 588:4165-4175.
15. Hirsch J.A., Martinez L.M., Pillai C., Alonso J.-M., Wang Q., Sommer F.T. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat Neurosci 2003, 6:1300-1308.
16. Runyan C.A., Schummers J., Van Wart A., Kuhlman S.J., Wilson N.R., Huang Z.J., Sur M. Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 2010, 67:847-857.
17. Zariwala H.A., Madisen L., Ahrens K.F., Bernard A., Lein E.S., Jones A.R., Zeng H. Visual tuning properties of genetically identified layer 2/3 neuronal types in the primary visual cortex of cre-transgenic mice. Front Syst Neurosci 2011, 4:162.
18. 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 2010, 67:858-871.
19. Monier C., Chavane F., Baudot P., Graham L.J., Frégnac Y. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 2003, 37:663-680.
20. Atallah B.V., Bruns W., Carandini M., Scanziani M. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 2012, 73:159-170.
21. Wilson N.R., Runyan C.A., Wang F.L., Sur M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 2012, 488:343-348.
22. Lee S-H., Kwan A.C., Zhang S., Phoumthipphavong V., Flannery J.G., Masmanidis S.C., Taniguchi H., Huang Z.J., Zhang F., Boyden E.S., et al. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 2012, 488:379-383.
23. Adesnik H., Bruns W., Taniguchi H., Huang Z.J., Scanziani M. A neural circuit for spatial summation in visual cortex. Nature 2012, 490:226-231.
24. Nienborg H., Hasenstaub A., Nauhaus I., Taniguchi H., Huang Z.J., Callaway E.M. Contrast dependence and differential contributions from somatostatin- and parvalbumin-expressing neurons to spatial integration in mouse V1. J Neurosci 2013, 33:11145-11154.
25. Moore A.K., Wehr M. Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci 2013, 33:13713-13723.
26. Ascoli G.A., Alonso-Nanclares L., Anderson S.A., Barrionuevo G., Benavides-Piccione R., Burkhalter A., Buzsáki G., Cauli B., Defelipe J., Fairén A., et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 2008, 9:557-568.
27. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
28. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Kvitsani D., Fu Y., Lu J., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
29. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
30. Galarreta M., Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 1999, 402:72-75.
31. Hu H., Ma Y., Agmon A. Submillisecond firing synchrony between different subtypes of cortical interneurons connected chemically but not electrically. J Neurosci 2011, 31:3351-3361.
32. 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 2013, 16:1068-1076.
33. Tamás G., Buhl E.H., Lörincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 2000, 3:366-371.
34. Buzsáki G., Wang X-J. Mechanisms of gamma oscillations. Annu Rev Neurosci 2012, 35:203-225.
35. Basu J., Srinivas K.V., Cheung S.K., Taniguchi H., Huang Z.J., Siegelbaum S.A. A cortico-hippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow. Neuron 2013, 79:1208-1221.
36. Somogyi P. A specific axo-axonal interneuron in the visual cortex of the rat. Brain Res 1977, 136:345-350.
37. Szabadics J., Varga C., Molnár G., Oláh S., Barzó P., Tamás G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 2006, 311:233-235.
38. Glickfeld L.L., Roberts J.D., Somogyi P., Scanziani M. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat Neurosci 2009, 12:21-23.
39. Woodruff A.R., McGarry L.M., Vogels T.P., Inan M., Anderson S.A., Yuste R. State-dependent function of neocortical chandelier cells. J Neurosci 2011, 31:17872-17886.
40. Viney T.J., Lasztoczi B., Katona L., Crump M.G., Tukker J.J., Klausberger T., Somogyi P. Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo. Nat Neurosci 2013, 16:1802-1811.
41. Taniguchi H., Lu J., Huang Z.J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 2013, 339:70-74.
42. Cottam J.C.H., Smith S.L., Hausser M. Target-specific effects of somatostatin-expressing interneurons on neocortical visual processing. J Neurosci 2013, 33:19567-19578.
43. Silberberg G., Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 2007, 53:735-746.
44. Kapfer C., Glickfeld L.L., Atallah B.V., Scanziani M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 2007, 10:743-753.
45. Chiu C.Q., Lur G., Morse T.M., Carnevale N.T., Ellis-Davies G.C.R., Higley M.J. Compartmentalization of GABAergic inhibition by dendritic spines. Science 2013, 340:759-762.
46. Xu H., Jeong H-Y., Tremblay R., Rudy B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 2013, 77:155-167.
47. Fino E., Yuste R. Dense inhibitory connectivity in neocortex. Neuron 2011, 69:1188-1203.
48. Letzkus J.J., Wolff S.B.E., Meyer E.M.M., Tovote P., Courtin J., Herry C., Lüthi A. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 2011, 480:331-335.
49. Jiang X., Wang G., Lee A.J., Stornetta R.L., Zhu J.J. The organization of two new cortical interneuronal circuits. Nat Neurosci 2013, 16:210-218.
50. Pi H-J., Hangya B., Kvitsiani D., Sanders J.I., Huang Z.J., Kepecs A. Cortical interneurons that specialize in disinhibitory control. Nature 2013, 503:521-524.
51. Lee S., Kruglikov I., Huang Z.J., Fishell G., Rudy B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci 2013, 16:1662-1670.
52. Acsády L., Görcs T.J., Freund T.F. Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 1996, 73:317-334.
53. Hajos N., Acsady L., Freund T.F. Target selectivity and neurochemical characteristics of VIP-immunoreactive interneurons in the rat dentate gyrus. Eur J Neurosci 1996, 8:1415-1431.
54. Dávid C., Schleicher A., Zuschratter W., Staiger J.F. The innervation of parvalbumin-containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat. Eur J Neurosci 2007, 25:2329-2340.
55. Donato F., Rompani S.B., Caroni P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 2013, 504:272-276.
56. Narayanan N.S., Laubach M. Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron 2006, 52:921-931.
57. Hromádka T., Deweese M.R., Zador A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 2008, 6:e16.
58. Churchland M.M., Shenoy K.V. Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J Neurophysiol 2007, 97:4235-4257.
59. Machens C.K., Romo R., Brody C.D. Functional, but not anatomical, separation of what and when in prefrontal cortex. J Neurosci 2010, 30:350-360.
60. Mante V., Sussillo D., Shenoy K.V., Newsome W.T. Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 2013, 503:78-84.
61. Maass W., Natschläger T., Markram H. Real-time computing without stable states: a new framework for neural computation based on perturbations. Neural Comput 2002, 14:2531-2560.
62. Sussillo D., Abbott L.F. Generating coherent patterns of activity from chaotic neural networks. Neuron 2009, 63:544-557.
63. Chelaru M.I., Dragoi V. Efficient coding in heterogeneous neuronal populations. Proc Natl Acad Sci U S A 2008, 105:16344-16349.
64. Xu X., Roby K.D., Callaway E.M. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 2010, 518:389-404.
65. Csicsvari J., Hirase H., Czurko A., Mamiya A., Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 1999, 19:274-287.
66. Bartho P., Hirase H., Monconduit L., Zugaro M., Harris K.D., Buzsaki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 2004, 92:600-608.
67. Klausberger T., Magill P.J., Márton L.F., Roberts J.D.B., Cobden P.M., Buzsáki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 2003, 421:844-848.
68. Fujisawa S., Amarasingham A., Harrison M.T., Buzsáki G. Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci 2008, 11:823-833.
69. Lee A.K., Manns I.D., Sakmann B., Brecht M. Whole-cell recordings in freely moving rats. Neuron 2006, 51:399-407.
70. Harvey C.D., Collman F., Dombeck D.A., Tank D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 2009, 461:941-946.
71. Lapray D., Lasztoczi B., Lagler M., Viney T.J., Katona L., Valenti O., Hartwich K., Borhegyi Z., Somogyi P., Klausberger T. Behavior-dependent specialization of identified hippocampal interneurons. Nat Neurosci 2012, 15:1265-1271.
72. Long M.A., Lee A.K. Intracellular recording in behaving animals. Curr Opin Neurobiol 2012, 22:34-44.
73. Sullivan D., Ozen S., Buzsaki G. Juxtacellular recording and labeling in the hippocampal dentate gyrus of freely moving rats. SFN abstract 2008, 435.2/H7.
74. Isomura Y., Harukuni R., Takekawa T., Aizawa H., Fukai T. Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 2009, 12:1586-1593.
75. Lima S.Q., Hromádka T., Znamenskiy P., Zador A.M. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS ONE 2009, 4:e6099.
76. Cohen J.Y., Haesler S., Vong L., Lowell B.B., Uchida N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 2012, 482:85-88.
77. Zhang F., Vierock J., Yizhar O., Fenno L.E., Tsunoda S., Kianianmomeni A., Prigge M., Berndt A., Cushman J., Polle J., et al. The microbial opsin family of optogenetic tools. Cell 2011, 147:1446-1457.
78. Courtin J., Chaudun F., Rozeske R.R., Karalis N., Gonzalez-Campo C., Wurtz H., Abdi A., Baufreton J., Bienvenu T.C.M., Herry C. Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 2013, 10.1038/nature12755.
79. Gentet L.J., Kremer Y., Taniguchi H., Huang Z.J., Staiger J.F., Petersen C.C.H. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci 2012, 15:607-612.
80. Paspalas C.D., Papadopoulos G.C. Serotoninergic afferents preferentially innervate distinct subclasses of peptidergic interneurons in the rat visual cortex. Brain Res 2001, 891:158-167.
81. Kawaguchi Y. Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 1997, 78:1743-1747.
82. Arroyo S., Bennett C., Aziz D., Brown S.P., Hestrin S. Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons. J Neurosci 2012, 32:3859-3864.
83. Alitto H.J., Dan Y. Cell-type-specific modulation of neocortical activity by basal forebrain input. Front Syst Neurosci 2012, 6:79.
84. Varga V., Losonczy A., Zemelman B.V., Borhegyi Z., Nyiri G., Domonkos A., Hangya B., Holderith N., Magee J.C., Freund T.F. Fast synaptic subcortical control of hippocampal circuits. Science 2009, 326:449-453.
85. Cauli B., Tong X.K., Rancillac A., Serluca N., Lambolez B., Rossier J., Hamel E. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci. 2004, 24:8940-8949.
86. Caputi A., Rozov A., Blatow M., Monyer H. Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. Cereb Cortex 2009, 19:1345-1359.
87. Gulyás A.I., Hájos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 1996, 16:3397-3411.
88. Fuentealba P., Tomioka R., Dalezios Y., Márton L.F., Studer M., Rockland K., Klausberger T., Somogyi P. Rhythmically active enkephalin-expressing GABAergic cells in the CA1 area of the hippocampus project to the subiculum and preferentially innervate interneurons. J Neurosci 2008, 28:10017-10022.