Influence of a subtype of inhibitory interneuron on stimulus-specific responses in visual cortex

Cerebral Cortex

Volumn 22, Issue 3, 2012, Pages 493-508

  Mao, Rong ^a   Schummers, James ^a   Knoblich, Ulf ^a,b   Lacey, Carolyn J ^c   Van Wart, Audra ^a   Cobos, Inma ^d   Kim, Carol ^d   Huguenard, John R ^c   Rubenstein, John L R ^d   Sur, Mriganka ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cortex; dendrite; inhibition; orientation; tuning

Indexed keywords

CALRETININ; NEUROPEPTIDE Y; SOMATOSTATIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; CONTROLLED STUDY; DENDRITE; INTERNEURON; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOUSE; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTIVE FIELD; REVIEW; STIMULUS RESPONSE; THALAMOCORTICAL TRACT; THALAMUS; VISUAL CORTEX; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; CELL COMMUNICATION; DOWN-REGULATION; HOMEODOMAIN PROTEINS; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; SEQUENCE DELETION; TRANSCRIPTION FACTORS; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 84863128033     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr057     Document Type: Review

References (98)

1. Allison JD, Kabara JF, Snider RK, Casagrande VA, Bonds AB. 1996. GABAB-receptor-mediated inhibition reduces the orientation selectivity of the sustained response of striate cortical neurons in cats. Vis Neurosci. 13(3):559-566. (Pubitemid 126673062)
2. Anderson JS, Carandini M, Ferster D. 2000. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol. 84(2):909-926. (Pubitemid 30655612)
3. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science. 278(5337):474-476. (Pubitemid 27454433)
4. Antonini A, Fagiolini M, Stryker MP. 1999. Anatomical correlates of functional plasticity in mouse visual cortex. J Neurosci. 19(11): 4388-4406. (Pubitemid 29241091)
5. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci. 9(7): 557-568. (Pubitemid 351873463)
6. Azouz R, Gray CM, Nowak LG, McCormick DA. 1997. Physiological properties of inhibitory interneurons in cat striate cortex. Cereb Cortex. 7(6):534-545. (Pubitemid 27353638)
7. Beierlein M, Gibson JR, Connors BW. 2003. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol. 90(5):2987-3000. (Pubitemid 37430000)
8. Benardo LS. 1994. Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro. J Physiol. 476(2):203-215. (Pubitemid 24129804)
9. Blatow M, Caputi A, Monyer H. 2005. Molecular diversity of neocortical GABAergic interneurones. J Physiol. 562(Pt 1):99-105. (Pubitemid 40207789)
10. Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JL. 1993. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci. 13(7):3155-3172. (Pubitemid 23199240)
11. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G. 2005. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron. 48(4):591-604. (Pubitemid 41654681)
12. Butt SJ, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G, Kimura S, Fishell G. 2008. The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron. 59(5):722-732.
13. Caputi A, Rozov A, Blatow M, Monyer H. 2008. Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. Cereb Cortex. 19(6):1345-1359.
14. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 459(7247): 663-667.
15. Cardin JA, Palmer LA, Contreras D. 2007. Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex. J Neurosci. 27(39):10333-10344. (Pubitemid 47502000)
16. Chen Y, Martinez-Conde S, Macknik SL, Bereshpolova Y, Swadlow HA, Alonso JM. 2008. Task difficulty modulates the activity of specific neuronal populations in primary visual cortex. Nat Neurosci. 11(8):974-982.
17. Chow A, Erisir A, Farb C, Nadal MS, Ozaita A, Lau D, Welker E, Rudy B. 1999. K(+) channel expression distinguishes subpopulations of parvalbumin-and somatostatin-containing neocortical interneurons. J Neurosci. 19(21):9332-9345. (Pubitemid 30228087)
18. Chung S, Ferster D. 1998. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron. 20(6):1177-1189. (Pubitemid 28293134)
19. Cobos I, Borello U, Rubenstein JL. 2007. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron. 54(6):873-888. (Pubitemid 46907500)
20. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL. 2005. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci. 8(8):1059-1068. (Pubitemid 41061517)
21. Connors BW, Malenka RC, Silva LR. 1988. Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J Physiol. 406:443-468.
22. DeFelipe J. 1993. Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb Cortex. 3(4):273-289.
23. Destexhe A, Mainen ZF, Sejnowski TJ. 1994. Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci. 1(3):195-230.
24. Drager UC. 1974. Autoradiography of tritiated proline and fucose transported transneuronally from the eye to the visual cortex in pigmented and albino mice. Brain Res. 82(2):284-292.
25. Dragoi V, Sharma J, Sur M. 2000. Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron. 28(1):287-298.
26. Eysel UT, Shevelev IA, Lazareva NA, Sharaev GA. 1998. Orientation tuning and receptive field structure in cat striate neurons during local blockade of intracortical inhibition. Neuroscience. 84(1):25-36. (Pubitemid 28081522)
27. Fagiolini M, Fritschy JM, Low K, Mohler H, Rudolph U, Hensch TK. 2004. Specific GABAA circuits for visual cortical plasticity. Science. 303(5664):1681-1683. (Pubitemid 38338328)
28. Ferster D, Chung S, Wheat H. 1996. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature. 380(6571): 249-252. (Pubitemid 26090647)
29. Ferster D, Miller KD. 2000. Neural mechanisms of orientation selectivity in the visual cortex. Annu Rev Neurosci. 23:441-471. (Pubitemid 30350050)
30. Finn IM, Priebe NJ, Ferster D. 2007. The emergence of contrastinvariant orientation tuning in simple cells of cat visual cortex. Neuron. 54(1):137-152. (Pubitemid 46498685)
31. Galarreta M, Erdelyi F, Szabo G, Hestrin S. 2004. Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci. 24(44):9770-9778. (Pubitemid 39463558)
32. Golomb D, Amitai Y. 1997. Propagating neuronal discharges in neocortical slices: computational and experimental study. J Neurophysiol. 78(3):1199-1211. (Pubitemid 27400663)
33. Gonchar Y, Burkhalter A. 1999. Connectivity of GABAergic calretininimmunoreactive neurons in rat primary visual cortex. Cereb Cortex. 9(7):683-696. (Pubitemid 29514098)
34. Gonchar Y, Wang Q, Burkhalter A. 2007. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. 1:3.
35. Hirsch JA, Martinez LM, Pillai C, Alonso JM, Wang Q, Sommer FT. 2003. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat Neurosci. 6(12):1300-1308. (Pubitemid 37485124)
36. Hubener M. 2003. Mouse visual cortex. Curr Opin Neurobiol. 13(4):413-420. (Pubitemid 37088230)
37. Jirmann KU, Pernberg J, Eysel UT. 2009. Region-specificity of GABAA receptor mediated effects on orientation and direction selectivity in cat visual cortical area 18. Exp Brain Res. 192(3):369-378.
38. Jones EG, Rubenstein JL. 2004. Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. J Comp Neurol. 477(1):55-80. (Pubitemid 39038180)
39. Kang Y, Kaneko T, Ohishi H, Endo K, Araki T. 1994. Spatiotemporally differential inhibition of pyramidal cells in the cat motor cortex. J Neurophysiol. 71(1):280-293. (Pubitemid 24058858)
40. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M. 2007. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci. 10(6):743-753. (Pubitemid 46828515)
41. Karagiannis A, Gallopin T, David C, Battaglia D, Geoffroy H, Rossier J, Hillman EM, Staiger JF, Cauli B. 2009. Classification of NPYexpressing neocortical interneurons. J Neurosci. 29(11):3642-3659.
42. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex. 7(6):476-486. (Pubitemid 27353633)
43. Kawaguchi Y, Kubota Y. 1998. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience. 85(3):677-701. (Pubitemid 28223633)
44. Kerlin AM, Andermann ML, Berezovskii VK, Reid RC. 2010. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron. 67(5):858-871.
45. Kubota Y, Kawaguchi Y. 1997. Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons. Brain Res. 752(1-2):175-183. (Pubitemid 27143911)
46. Lauritzen TZ, Miller KD. 2003. Different roles for simple-cell and complex-cell inhibition in V1. J Neurosci. 23(32):10201-10213. (Pubitemid 37444596)
47. Liodis P, Denaxa M, Grigoriou M, Akufo-Addo C, Yanagawa Y, Pachnis V. 2007. Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J Neurosci. 27(12):3078-3089. (Pubitemid 46474122)
48. Liu BH, Li P, Li YT, Sun YJ, Yanagawa Y, Obata K, Zhang LI, Tao HW. 2009. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J Neurosci. 29(34):10520-10532.
49. Luo L, Callaway EM, Svoboda K. 2008. Genetic dissection of neural circuits. Neuron. 57(5):634-660. (Pubitemid 351335341)
50. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A. 2006. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci. 26(19):5069-5082. (Pubitemid 44315288)
51. Marin O, Rubenstein JL. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci. 2(11):780-790. (Pubitemid 33674060)
52. Marino J, Schummers J, Lyon DC, Schwabe L, Beck O, Wiesing P, Obermayer K, Sur M. 2005. Invariant computations in local cortical networks with balanced excitation and inhibition. Nat Neurosci. 8(2):194-201. (Pubitemid 40194050)
53. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 5(10):793-807. (Pubitemid 39336216)
54. Meskenaite V. 1997. Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol. 379(1):113-132. (Pubitemid 27114196)
55. Mitchell JF, Sundberg KA, Reynolds JH. 2007. Differential attentiondependent response modulation across cell classes in macaque visual area V4. Neuron. 55(1):131-141. (Pubitemid 46990821)
56. Monier C, Chavane F, Baudot P, Graham LJ, Fregnac Y. 2003. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron. 37(4):663-680. (Pubitemid 36262987)
57. Murayama M, Perez-Garci E, Nevian T, Bock T, Senn W, Larkum ME. 2009. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature. 457(7233):1137-1141.
58. Mutch J, Knoblich U, Poggio T. 2010. CNS: a GPU-based framework for simulating cortically-organized networks. Cambridge (MA): Massachusetts Institute of Technology MIT-CSAIL-TR-2010-013/CBCL-286.
59. Nelson S, Toth L, Sheth B, Sur M. 1994. Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science. 265(5173):774-777. (Pubitemid 24266135)
60. Newberry NR, Nicoll RA. 1985. Comparison of the action of baclofen with gamma-aminobutyric acid on rat hippocampal pyramidal cells in vitro. J Physiol. 360:161-185. (Pubitemid 15133990)
61. Niell CM, Stryker MP. 2008. Highly selective receptive fields in mouse visual cortex. J Neurosci. 28(30):7520-7536.
62. Nowak LG, Sanchez-Vives MV, McCormick DA. 2008. Lack of orientation and direction selectivity in a subgroup of fast-spiking inhibitory interneurons: cellular and synaptic mechanisms and comparison with other electrophysiological cell types. Cereb Cortex. 18(5):1058-1078.
63. Otis TS, Mody I. 1992. Differential activation of GABAA and GABAB receptors by spontaneously released transmitter. J Neurophysiol. 67(1):227-235.
64. Palmer SE, Miller KD. 2007. Effects of inhibitory gain and conductance fluctuations in a simple model for contrast-invariant orientation tuning in cat V1. J Neurophysiol. 98(1):63-78. (Pubitemid 47084799)
65. Palop JJ, Roberson ED, Cobos I. 2010. Step-by-step in situ hybridization method for localizing gene expression changes in the brain. Methods Mol Biol. 670:207-230.
66. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego (CA): Academic Press.
67. Pfleger B, Bonds AB. 1995. Dynamic differentiation of GABAA-sensitive influences on orientation selectivity of complex cells in the cat striate cortex. Exp Brain Res. 104(1):81-88.
68. Priebe NJ, Ferster D. 2008. Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron. 57(4):482-497. (Pubitemid 351274000)
69. Qiu M, Bulfone A, Ghattas I, Meneses JJ, Christensen L, Sharpe PT, Presley R, Pedersen RA, Rubenstein JL. 1997. Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and-2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev Biol. 185(2):165-184. (Pubitemid 27226825)
70. Racine RJ. 1972. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 32(3):281-294.
71. Runyan CA, Schummers J, Van Wart A, Kuhlman SJ, Wilson NR, Huang ZJ, Sur M. 2010. Response features of parvalbuminexpressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron. 67(5):847-857.
72. Schummers J, Cronin B, Wimmer K, Stimberg M, Martin R, Obermayer K, Koerding K, Sur M. 2007. Dynamics of orientation tuning in cat v1 neurons depend on location within layers and orientation maps. Front Neurosci. 1(1):145-159.
73. Schummers J, Marino J, Sur M. 2002. Synaptic integration by V1 neurons depends on location within the orientation map. Neuron. 36(5):969-978. (Pubitemid 35447867)
74. Segal M. 1990. A subset of local interneurons generate slow inhibitory postsynaptic potentials in hippocampal neurons. Brain Res. 511(1):163-164. (Pubitemid 20079233)
75. Shapley R, Hawken M, Ringach DL. 2003. Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron. 38(5):689-699. (Pubitemid 36694777)
76. Sherman SM, Koch C. 1986. The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res. 63(1):1-20. (Pubitemid 16064863)
77. Sherman SM, Spear PD. 1982. Organization of visual pathways in normal and visually deprived cats. Physiol Rev. 62(2):738-855.
78. Silberberg G, Markram H. 2007. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron. 53(5):735-746.
79. Sillito AM. 1975. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol. 250(2):305-329.
80. Sillito AM. 1977. The spatial extent of excitatory and inhibitory zones in the receptive field of superficial layer hypercomplex cells. J Physiol. 273(3):791-803. (Pubitemid 8251504)
81. Sohal VS, Zhang F, Yizhar O, Deisseroth K. 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 459(7247):698-702.
82. Sohya K, Kameyama K, Yanagawa Y, Obata K, Tsumoto T. 2007. GABAergic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2+ imaging in transgenic mice. J Neurosci. 27(8):2145-2149.
83. Soltesz I, Crunelli V. 1992. GABAA and pre-and post-synaptic GABAB receptor-mediated responses in the lateral geniculate nucleus. Prog Brain Res. 90:151-169.
84. Somers DC, Nelson SB, Sur M. 1995. An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci. 15(8):5448-5465.
85. Sugita S, Johnson SW, North RA. 1992. Synaptic inputs to GABAA and GABAB receptors originate from discrete afferent neurons. Neurosci Lett. 134(2):207-211.
86. Sussel L, Marin O, Kimura S, Rubenstein JL. 1999. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development. 126(15):3359-3370. (Pubitemid 29396776)
87. Swindale NV. 1998. Orientation tuning curves: empirical description and estimation of parameters. Biol Cybern. 78(1):45-56. (Pubitemid 128636373)
88. Tamas G, Lorincz A, Simon A, Szabadics J. 2003. Identified sources and targets of slow inhibition in the neocortex. Science. 299(5614): 1902-1905. (Pubitemid 36356660)
89. Toledo-Rodriguez M, Blumenfeld B, Wu C, Luo J, Attali B, Goodman P, Markram H. 2004. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb Cortex. 14(12):1310-1327. (Pubitemid 39507282)
90. Varela JA, Sen K, Gibson J, Fost J, Abbott LF, Nelson SB. 1997. A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci. 17(20):7926-7940. (Pubitemid 27426228)
91. Vidyasagar TR, Pei X, Volgushev M. 1996. Multiple mechanisms underlying the orientation selectivity of visual cortical neurones. Trends Neurosci. 19(7):272-277. (Pubitemid 26000674)
92. Wang XJ, Buzsaki G. 1996. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci. 16(20):6402-6413. (Pubitemid 26337364)
93. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. 2002. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex. 12(4):395-410. (Pubitemid 34226064)
94. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci. 7(9):687-696. (Pubitemid 44267493)
95. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. 2004. Origins of cortical interneuron subtypes. J Neurosci. 24(11):2612-2622. (Pubitemid 38380937)
96. Xu X, Roby KD, Callaway EM. 2006. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol. 499(1):144-160. (Pubitemid 44423701)
97. Yazaki-Sugiyama Y, Kang S, Cateau H, Fukai T, Hensch TK. 2009. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature. 462(7270):218-221.
98. Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL. 2008. Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol. 510(1):79-99.