Trajectory of the main GABAergic interneuron populations from early development to old age in the rat primary auditory cortex

Frontiers in Neuroanatomy

Volumn 8, Issue JUN, 2014, Pages

  Ouellet, Lydia ^a   de Villers Sidani, Etienne ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

A1; Aging; Auditory; GABA; Inhibition; Interneurons; Parvalbumin; Somatostatin

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; BIOLOGICAL MARKER; CALRETININ; CHOLECYSTOKININ; CHOLINE ACETYLTRANSFERASE; NEUROPEPTIDE Y; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

AGE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; CELL COUNT; CELLULAR DISTRIBUTION; COGNITION; CORTICAL THICKNESS (BRAIN); GABAERGIC TRANSMISSION; IMMUNOHISTOLOGY; INTERNEURON; LEARNING; MICROPHOTOGRAPHY; MICROSCOPY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; RAT;

EID: 84901831891     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00040     Document Type: Article

References (106)

1. Akbarian, S., Kim, J. J., Potkin, S. G., Hagman, J. O., Tafazzoli, A., Bunney, W. E., et al. (1995). Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch. Gen. Psychiatry52, 258-266. doi: 10.1001/archpsyc.1995.03950160008002
2. Anderson, S. A., Kaznowski, C. E., Horn, C., Rubenstein, J. L., and McConnell, S. K. (2002). Distinct origins of neocortical projection neurons and interneuronsin vivo. Cereb. Cortex12, 702-709. doi: 10.1093/cercor/12.7.702
3. Anomal, R., de Villers-Sidani, E., Merzenich, M. M., and Panizzutti, R. (2013). Manipulation of BDNF signaling modifies the experience-dependent plasticity induced by pure tone exposure during the critical period in the primary auditory cortex. PLoS ONE8:e64208. doi: 10.1371/journal.pone.0064208
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. Bartolini, G., Ciceri, G., and Marin, O. (2013). Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults. Neuron79, 849-864. doi: 10.1016/j.neuron.2013.08.014
6. Bartos, M., Vida, I., and Jonas, P. (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneurons networks. Nat. Rev. Neurosci. 8, 45-56. doi: 10.1038/nrn2044
7. Bao, S., Chang, E. F., Davis, J. D., Gobeske, K. T., and Merzenich, M. M. (2003). Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex.J. Neurosci. 23, 10765-10775.
8. Beaulieu, C. (1993). Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res. 609, 284-292. doi: 10.1016/0006-8993(93)90884-P
9. Areceptor binding on neurons of the prefrontal cortex in schizophrenic subjects. Neuroscience75, 1021-1031. doi: 10.1016/0306-4522(96)00328-4
10. Beierlein, M., Gibson, J. R., and Connors, B. W. (2000). A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3, 904-910. doi: 10.1038/78809
11. Borbély, E., Scheich, B., and Helyes, Z. (2013). Neuropeptides in learning and memory. Neuropeptides47, 439-450. doi: 10.1016/j.npep.2013.10.012
12. Bu, J., Sathyendra, V., Nagykery, N., and Geula, C. (2003). Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp. Neurol. 182, 220-231. doi: 10.1016/S0014-4886(03)00094-3
13. Burianova, J., Ouda, L., Profant, O., and Syka, J. (2009). Age-related changes in GAD levels in the central auditory system of the rat. Exp. Gerontol. 44, 161-169. doi: 10.1016/j.exger.2008.09.012
14. Butt, S. J., Fuccillo, M., Nery, S., Noctors, S., Kriegstein, A., Corbin, J. G., et al. (2005). The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neurons48, 591-604. doi: 10.1016/j.neuron.2005.09.034
15. Caballero, A., Diah, K. C., and Tseng, K. Y. (2013). Region-specific upregulation of parvalbumin-, but not calretinin-positive cells in the ventral hippocampus during adolescence. Hippocampus23, 1331-1336. doi: 10.1002/hipo.22172
16. Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., et al. (2009). Driving fast-spiking cells induce gamma rhythm and controls sensory responses. Nature459, 663-667. doi: 10.1038/nature08002
17. Caspary, D. M., Ling, L., Turner, J. G., and Hughes, L. F. (2008). Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system.J. Exp. Biol. 211, 1781-1791. doi: 10.1242/jeb.013581
18. Cha, C. I., Lee, E. Y., Park, K. H., and Baik, S. H. (1997). Age-related changes of VIP, NPY and somatostatin-immunoreactive neurons in the cerebral cortex of aged rats. Brain Res. 753, 235-244. doi: 10.1016/S0006-8993(97)00009-7
19. Cha, C. I., Lee, Y. I., and Baik, S. H. (1996). Age-related change of neuropeptide Y-immunoreactive neurons in the cerebral cortex of aged rats. Neurosci. Lett. 214, 37-40. doi: 10.1016/0304-3940(96)12876-7
20. Chang, E. F., Bao, S., Imaizumi, K., Schreiner, C. E., and Merzenich, M. M. (2005). Development of spectral and temporal response selectivity in the auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 102, 16460-16465. doi: 10.1073/pnas.0508239102
21. Cossart, R., Dinocourt, C., Hirsch, J. C., Merchan-Perez, A., De Felipe, J., Ben-Ari, Y., et al. (2001). Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 4, 52-62. doi: 10.1038/82900
22. Dani, V. S., Chang, Q., Maffe, A., Turrigiano, G. G., Jaenisch, R., and Nelson, S. B. (2005). Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett Syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 12560-12565. doi: 10.1073/pnas.0506071102
23. DeFelipe, J. (1993). Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium binding proteins, and cell surface molecules. Cereb. Cortex3, 273-289. doi: 10.1093/cercor/3.4.273
24. DeFelipe, J., Lopez-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larranaga, P., Anderson, S., et al. (2013). New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14, 202-216. doi: 10.1038/nrn3444
25. Del Campo, C. H. N., Measor, K. R., and Razak, K. A. (2012). Parvalbuminimmunoreactivity in the auditory cortex of a mouse model of presbycusis. Hear. Res. 294, 31-39. doi: 10.1016/j.heares.2012.08.017
26. Del Rio, M. R., and DeFelipe, J. (1997). Colocalization of parvalbumin and calbindin D-28k in neurons including chandelier cells of the human temporal cortex.J. Chem. Neuroanat. 12, 165-173. doi: 10.1016/S0891-0618(96)00191-3
27. de Villers-Sidani, E., Alzghoul, L., Zhou, X., Simpson, K. L., Lin, R. C., and Merzenich, M. M. (2010). Recovery of functional and structural age-related changes in the rat primary auditory cortex with operant training. Proc. Natl. Acad. Sci. U.S.A. 107, 13900-13905. doi: 10.1073/pnas.1007885107
28. de Villers-Sidani, E., Chang, E. F., Bao, S. B., and Merzenich, M. M. (2007). Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat.J. Neurosci. 27, 180-189. doi: 10.1523/JNEUROSCI.3227-06.2007
29. de Villers-Sidani, E., and Merzenich, M. M. (2011). Lifelong plasticity in the rat auditory cortex: basic mechanisms and role of sensory experience. Prog. Brain Res. 191, 119-131. doi: 10.1016/B978-0-444-53752-2.00009-6
30. de Villers-Sidani, E., Simpson, K. L., Lu, Y. F., Lin, R. C. S., and Merzenich, M. M. (2008). Manipulating critical period closure across different sectors of the primary auditory cortex. Nat. Neurosci. 11, 957-965. doi: 10.1038/nn.2144
31. Dreifuss, J. J., Kelly, J. S., and Krnjevic, K. (1969). Cortical inhibition and gamma-aminobutyric acid. Exp. Brain Res. 9, 137-154. doi: 10.1007/BF00238327
32. Fagiolini, M., and Hensch, T. K. (2000). Inhibitory threshold for critical-period activation in primary visual cortex. Nature404, 183-186. doi: 10.1038/35004582
33. Fish, K. N., Hoftman, G. D., Sheikh, W., Kitchens, M., and Lewis, D. A. (2013). Parvalbumin-containing chandelier and basket cell boutons have distinctive modes of maturation in monkey prefrontal cortex.J. Neurosci. 33, 8352-8358. doi: 10.1523/JNEUROSCI.0306-13.2013
34. Fitzpatrick, D., Lund, J. S., Schmechel, D. E., and Towles, A. C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex.J. Comp. Neurol. 264, 73-91. doi: 10.1002/cne.902640107
35. Fries, P., Schröder, J. H., Roelfsema, P. R., Singer, W., and Engel, A. K. (2002). Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection.J. Neurosci. 22, 3739-3754.
36. Froemke, R. C., Merzenich, M. M., and Schreiner, C. E. (2007). A synaptic memory trace for cortical receptive field plasticity. Nature450, 425-429. doi: 10.1038/nature06289
37. Fox, K., and Wong, O. L. (2005). A comparison of experience-dependant plasticity in the visual and somatosensory system. Neuron48, 465-477. doi: 10.1016/j.neuron.2005.10.013
38. Games, K. D., and Winer, J. A. (1988). Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hear. Res. 34, 1-25. doi: 10.1016/0378-5955(88)90047-0
39. Gelman, D. M., and Marin, O. (2010). Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 31, 2136-2141. doi: 10.1111/j.1460-9568.2010.07267.x
40. Giacobini, P., and Wray, S. (2008). Prenatal expression of cholecystokinin (CCK) in the central nervous system (CNS) of mouse. Neurosci. Lett. 438, 96-101. doi: 10.1016/j.neulet.2008.04.042
41. Gonchar, Y., and Burkhalter, A. (1997). Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex7, 347-358. doi: 10.1093/cercor/7.4.347
42. Gonchar, Y., Wang, Q., and Burkhalter, A. (2008). Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 1:3. doi: 10.3389/neuro.05.003.2007
43. Hazra, A., Gu, F., Aulakh, A., Berridge, C., Eriksen, J. L., and Žiburkus, J. (2013). Inhibitory neuron and hippocampal circuit dysfunction in an aged mouse model of alzheimer's disease. PLoS ONE8:e64318. doi: 10.1371/journal.pone.0064318
44. Hendry, S. H., Schwark, H. D., Jones, E. G., and Yan, J. (1987). Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex.J. Neurosci. 7, 1503-1519.
45. Hensch, T. K. (2004). Critical period regulation. Annu. Rev. Neurosci. 27, 549-579. doi: 10.1146/annurev.neuro.27.070203.144327
46. Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888. doi: 10.1038/nrn1787
47. Hensch, T. K., Fagiolini, M., Mataga, N., Stryker, M. P., Baekkeskov, S., and Kash, S. F. (1998). Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science282, 1504-1508. doi: 10.1126/science.282.5393.1504
48. Hof, P. R., Glezer, I. I., Condé, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., et al. (1999). Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns.J. Chem. Neuroanat. 16, 77-116. doi: 10.1016/S0891-0618(98)00065-9
49. Kamal, B., Holman, C., and de Villers-Sidani, E. (2013). Shaping the aging brain: role of auditory input patterns in the emergence of auditory cortical impairments. Front. Syst. Neurosci. 7:52. doi: 10.3389/fnsys.2013.00052
50. Kowiański, P., Moryś, J. M., Wójcik, S., Dziewiatkowski, J., Luczyñska, A., Spodnik, E., et al. (2004). Neuropeptide-containing neurons in the endopiriform region of the rat: morphology and colocalization with calcium-binding proteins and nitric oxide synthase. Brain Res. 996, 97-110. doi: 10.1016/j.brainres.2003.10.020
51. Kubota, Y., Hattori, R., and Yui, Y. (1994). Three distinct subpopulations of GABA-ergic neurons in rat frontal agranular cortex. Brain Res. 649, 159-173. doi: 10.1016/0006-8993(94)91060-X
52. Lehmann, K., Steinecke, A., and Bolz, J. (2012). GABA through the ages: regulation of cortical function and plasticity by inhibitory interneurons. Neural Plasticity2012:892784. doi: 10.1155/2012/892784
53. Letinic, K., Zoncu, R., and Rakic, P. (2002). Origin of GABAergic neurons in the human neocortex. Nature417, 645-649. doi: 10.1038/nature00779
54. 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. Nature480, 331-335. doi: 10.1038/nature10674
55. Levitt, P. (2005). Disruption of interneuron development. Epilepsia46, 22-28. doi: 10.1111/j.1528-1167.2005.00305.x
56. Levitt, P., Eagleson, K. L., and Powell, E. M. (2004). Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci. 27, 400-406. doi: 10.1016/j.tins.2004.05.008
57. Lewis, D. A. (2000). GABAergic local circuit neurons and prefrontal cortex dysfunction in schizophrenia. Brain Res. Rev. 31, 270-276. doi: 10.1016/S0165-0173(99)00042-9
58. Lewis, D. A., Hashimoto, T., and Volk, D. W. (2005). Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324 doi: 10.1038/nrn1648
59. Lin, L.-C., and Sibille, E. (2013). Reduced brain somatostatin in mood disorders: a common pathophysiological substrate and drug target?Front. Pharmacol. 4, 1-12. doi: 10.3389/fphar.2013.00110
60. Lin, S., Boey, D., and Herzog, H. (2004). NPY and Y receptors: lessons from transgenic and knockout models. Neuropeptides38, 189-200. doi: 10.1016/j.npep.2004.05.005
61. Linden, J. F. (2012). Consequences of chronic reduction of cortical inhibition. PNAS109, 13473-13474. doi: 10.1073/pnas.1210409109
62. Lowenstein, D. H., Thomas, M. J., Smith, D. H., and McIntosh, T. K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus.J. Neurosci. 12, 4846-4853.
63. Maffei, A., Nataraj, K., Nelson, S. B., and Turrigiano, G. G. (2006). Potentiation of cortical inhibition by visual deprivation. Nature443, 81-84. doi: 10.1038/nature05079
64. Marin, O. (2012). Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120. doi: 10.1038/nrn3155
65. 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
66. Martel, G., Dutar, P., Epelbaum, J., and Viollet, C. (2012). Somatostatinergic systems: an update on brain functions in normal and pathological aging. Front. Endocrinol. 3:154. doi: 10.3389/fendo.2012.00154
67. Martinez, L. M., Alonso, J. M., Reid, R. C., and Hirsch, J. A. (2002). Laminar processing of stimulus orientation in cat visual cortex.J. Physiol. 540, 321-333. doi: 10.1113/jphysiol.2001.012776
68. McBain, C. J., and Fisahn, A. (2001). Interneurons unbound. Nat. Rev. Neurosci. 2, 11-23. doi: 10.1038/35049047
69. Miettinen, R., Sirvio, J., Riekkinen, P., Laakso, M. P., Riekkinen, M., and Riekkinen, P. (1993). Neocortical, hippocampal and septalparvalbumin-and somatostatin-containing neurons in young and aged rats: correlation with passive avoidance and water maze performance. Neuroscience53, 367-378. doi: 10.1016/0306-4522(93)90201-P
70. Minthon, L., Edvinsson, L., and Gustafson, L. (1996). Correlation between clinical characteristics and cerebrospinal fluid neuropeptide Y levels in dementia of the Alzheimer type and frontotemporaldementia. Alzheimer Dis. Assoc. Disord. 10, 197-203.
71. Miyoshi, G., Butt, S. J. B., Takebayashi, H., and Fishell, G. (2007). Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalicOlig2-expressing precursors.J. Neurosci. 27, 7786-7798. doi: 10.1523/JNEUROSCI.1807-07.2007
72. Molnár, Z., Métin, C., Stoykova, A., Tarabykin, V., Price, D. J., Francis, F., et al. (2006). Comparative aspects of cerebral cortial development. Eur. J. Neurosci. 23, 921-934. doi: 10.1111/j.1460-9568.2006.04611.x
73. Morino, P., Herrara-Marschitz, M., Castel, M. N., Ungerstedt, U., Varro, A., Dockray, G., et al. (1994). Cholecystokinin in cortico-striatal neurons in the rat: immunohistochemical studies at the light and electron microscopical level. Eur. J. Neurosci. 6, 681-692. doi: 10.1111/j.1460-9568.1994.tb00980.x
74. Nakhate, K. T., Dandekar, M. P., Kokare, D. M., and Subhedar, N. K. (2009). Involvement of neuropeptide Y Y(1) receptors in the acute, chronic and withdrawal effects of nicotine on feeding and body weight in rats. Eur J. Pharmacol. 609, 78-87. doi: 10.1016/j.ejphar.2009.03.008
75. Ouda, L., Druga, R., and Syka, J. (2008). Changes in parvalbumin immunoreactivity with aging in the central auditory system of the rat. Exp. Gerontol. 43, 782-789. doi: 10.1016/j.exger.2008.04.001
76. Patel, Y. C. (1999). Somatostatin and its receptor family. Front. Neuroendocrinol. 20, 157-198. doi: 10.1006/frne.1999.0183
77. Pinto, J., Hornby, K., Jones, D., and Murphy, K. (2010). Developmental changes in GABAergic mechanisms in human visual cortex across the lifespan. Front. Cell. Neurosci. 4:16. doi: 10.3389/fncel.2010.00016
78. Pugliese, M., Carrasco, J. L., Geloso, M. C., Mascort, J., Michetti, F., and Mahy, N. (2004). Gamma-aminobutyric acidergic interneuron vulnerability to aging in canine prefrontal cortex.J. Neurosci. Res. 77, 913-920. doi: 10.1002/jnr.20223
79. Razak, K. A., and Fuzessery, Z. M. (2009). GABA shapes selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex.J. Neurophysiol. 102, 1366-1378. doi: 10.1152/jn.00334.2009
80. Rubenstein, J. H., and Merzenich, M. M. (2003). Model of autism: increase ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2, 255-267. doi: 10.1034/j.1601-183X.2003.00037.x
81. 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
82. Sanacora, G., Mason, G. F., and Krystal, J. H. (2000). Impairment of GABAergic transmission in depression: new insights from neuroimaging studies. Crit. Rev. Neurobiol. 14, 23-45. doi: 10.1615/CritRevNeurobiol.v14.i1.20
83. Schettini, G. (1991). Brain somatostatin: receptor-coupled transducing mechanisms and role in cognitive functions. Pharmacol. Res. 23, 203-215. doi: 10.1016/S1043-6618(05)80080-5
84. Schulze, H., and Langner, G. (1999). Auditory cortical responses to amplitude modulations with spectra above frequency receptive fields: evidence for wide spectral integration.J. Comp. Physiol. 185, 493-508. doi: 10.1007/s003590050410
85. Sohal, V. S., Zhang, F., Yizhar, O., and Deisseroth, K. (2009). Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature459, 698-702. doi: 10.1038/nature07991
86. Somogyi, P., Freund, T. F., Wu, J. Y., and Smith, A. D. (1983). The section-Golgi impregnation procedure. Immunocytochemical demonstration of glutamate decarboxylase in Golgi-impregnated neurons and in their afferent synaptic boutons in the visual cortex of the cat. Neuroscience9, 475-490. doi: 10.1016/0306-4522(83)90167-7
87. Somogyi, P., and Klausberger, P. (2005). Defined types of interneurone structure space and spike timing in the hippocampus.J. Physiol. 562, 9-26. doi: 10.1113/jphysiol.2004.078915
88. Stanley, E. M., Fadel, J. R., and Mott, D. D. (2012). Interneuron loss reduces dendritic inhibition and GABA release in hippocampus of aged rats. Neurobiol. Aging33, e1-431.13. doi: 10.1016/j.neurobiolaging.2010.12.014
89. Tallon-Baudry, C., Bertrand, O., Peronnet, F., and Pernier, J. (1998). Induced γ-band activity during the delay of a visual short term memory task in humans.J. Neurosci. 18, 4244-4254.
90. Tong, Z., Han, C., Luo, W., Li, H., Luo, H., Qiang, M., et al. (2013). Aging-associated excess formaldehyde leads to spatial memory deficits. Sci. Rep. 3, 1807. doi: 10.1038/srep01807
91. Valcanis, H., and Tan, S. S. (2003). Layer specification of transplanted interneurons in developing mouse neocortex.J. Neurosci. 23, 5113-5122.
92. Vecsei, L., and Widerlov, E. (1990). Preclinical and clinical studies with cysteamine and pantethine related to the central nervous system. Prog. Neuropsychopharmacol. Biol. Psychiatry14, 835-862.
93. Vela, J., Gutierrez, A., Vitorica, V., and Ruano, D. (2003). Rat hippocampal GABAergic molecular markers are differentially affected by ageing.J. Neurochem. 85, 368-377. doi: 10.1046/j.1471-4159.2003.01681.x
94. Verret, L., Mann, E. O., Hang, G. B., Barth, A. M. I., Cobos, I., Ho, K., et al. (2012). Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in alzheimer model. Cell149, 708-721. doi: 10.1016/j.cell.2012.02.046
95. Viollet, C., Lepousez, G., Loudes, C., Videau, C., Simon, A., and Epelbaum, J. (2008). Somatostatinergic systems in brain: networks and functions. Mol. Cell. Endocrinol. 286, 75-87. doi: 10.1016/j.mce.2007.09.007
96. 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/JNEUROSCI.4647-06.2007
97. Wehr, M., and Zador, A. M. (2003). Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature426, 442-446. doi: 10.1038/nature02116
98. Wonders, C. P., and Anderson, S. A. (2006). The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687-696. doi: 10.1038/nrn1954
99. 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. Neuron58, 132-143. doi: 10.1016/j.neuron.2008.01.035
100. Xu, Q., De La Cruz, E., Rubenstein, J. L., and Anderson, S. A. (2004). Origins of cortical interneuron subtypes.J. Neurosci. 24, 2612-2622. doi: 10.1523/JNEUROSCI.5667-03.2004
101. Xu, X., Roby, K. D., and Callaway, E. M. (2006). Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin.J. Comp. Neurol. 499, 144-160. doi: 10.1002/cne.21101
102. 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
103. Yan, Y.-H., Van Brederode, J. F. M., and Hendrickson, A. E. (1995). Transientco-localization of calretinin, parvalbumin, and calbindin-D28 in developing visual cortex of monkey.J. Neurocytol. 24, 825-837. doi: 10.1007/BF01179982
104. Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'Shea, D. J., et al. (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature477, 171-178. doi: 10.1038/nature10360
105. Yuste, R. (2005). Origin and classification of neocortical interneurons. Neuron48, 524-527. doi: 10.1016/j.neuron.2005.11.012
106. Zecevic, N., Hu, F., and Jakovcevski, I. (2011). Interneurons in the developing human neocortex. Dev. Neurobiol. 71, 18-33. doi: 10.1002/dneu.20812