Neurogenesis in the dentate gyrus: Carrying the message or dictating the tone

Frontiers in Neuroscience

Volumn , Issue 7 APR, 2013, Pages

  Piatti, Verónica C ^a   Ewe, Laura A ^a   Leutgeb, Jill K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dentate gyrus; Inhibition; Neurogenesis; Pattern separation; Sparse coding

Indexed keywords

ACTION POTENTIAL; CONNECTOME; DENTATE GYRUS; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; HUMAN; LONG TERM POTENTIATION; MEMORY; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REVIEW; SPATIAL DISCRIMINATION; TASK PERFORMANCE;

EID: 84878833143     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00050     Document Type: Review

References (110)

1. Acsady, L., and Kali, S. (2007). Models, structure, function: the transformation of cortical signals in the dentate gyrus. Prog. Brain Res. 163, 577-599.
2. Acsady, L., Kamondi, A., Sik, A., Freund, T., and Buzsaki, G. (1998). GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386-3403.
3. Aimone, J. B., Deng, W., and Gage, F. H. (2011). Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70, 589-596.
4. Alme, C. B., Buzzetti, R. A., Marrone, D. F., Leutgeb, J. K., Chawla, M. K., Schaner, M. J., et al. (2010). Hippocampal granule cells opt for early retirement. Hippocampus 20, 1109-1123.
5. Ambrogini, P., Lattanzi, D., Ciuffoli, S., Agostini, D., Bertini, L., Stocchi, V., et al. (2004). Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res. 1017, 21-31.
6. Barnes, C. A., McNaughton, B. L., Mizumori, S. J., Leonard, B. W., and Lin, L. H. (1990). Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog. Brain Res. 83, 287-300.
7. Boss, B. D., Peterson, G. M., and Cowan, W. M. (1985). On the number of neurons in the dentate gyrus of the rat. Brain Res. 338, 144-150.
8. Bramham, C. R., Worley, P. F., Moore, M. J., and Guzowski, J. F. (2008). The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J. Neurosci. 28, 11760-11767.
9. Burghardt, N. S., Park, E. H., Hen, R., and Fenton, A. A. (2012). Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 22, 1795-1808.
10. Burwell, R. D. (2000). The parahippocampal region: corticocortical connectivity. Ann. N.Y. Acad. Sci. 911, 25-42.
11. Cameron, H. A., and McKay, R. D. (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435, 406-417.
12. Campbell, N. R., Fernandes, C. C., Halff, A. W., and Berg, D. K. (2010). Endogenous signaling through alpha7-containing nicotinic receptors promotes maturation and integration of adult-born neurons in the hippocampus. J. Neurosci. 30, 8734-8744.
13. Chawla, M. K., Guzowski, J. F., Ramirez-Amaya, V., Lipa, P., Hoffman, K. L., Marriott, L. K., et al. (2005). Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15, 579-586.
14. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., et al. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213.
15. Creer, D. J., Romberg, C., Saksida, L. M., Van Praag, H., and Bussey, T. J. (2010). Running enhances spatial pattern separation in mice. Proc. Natl. Acad. Sci. U.S.A. 107, 2367-2372.
16. Dayer, A. G., Ford, A. A., Cleaver, K. M., Yassaee, M., and Cameron, H. A. (2003). Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol. 460, 563-572.
17. Dupret, D., Fabre, A., Dobrossy, M. D., Panatier, A., Rodriguez, J. J., Lamarque, S., et al. (2007). Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol. 5:e214. doi: 10.1371/journal.pbio.0050214
18. Durstewitz, D., Seamans, J. K., and Sejnowski, T. J. (2000). Neurocomputational models of working memory. Nat. Neurosci. 3(Suppl.), 1184-1191.
19. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., et al. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
20. Esposito, M. S., Piatti, V. C., Laplagne, D. A., Morgenstern, N. A., Ferrari, C. C., Pitossi, F. J., et al. (2005). Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25, 10074-10086.
21. Ewell, L. A., and Jones, M. V. (2010). Frequency-tuned distribution of inhibition in the dentate gyrus. J. Neurosci. 30, 12597-12607.
22. Faulkner, R. L., Jang, M. H., Liu, X. B., Duan, X., Sailor, K. A., Kim, J. Y., et al. (2008). Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc. Natl. Acad. Sci. U.S.A. 105, 14157-14162.
23. Freund, T. F., and Buzsaki, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
24. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438.
25. Ge, S., Goh, E. L., Sailor, K. A., Kitabatake, Y., Ming, G. L., and Song, H. (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589-593.
26. Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., and Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54, 559-566.
27. Gilbert, P. E., Kesner, R. P., and Lee, I. (2001). Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 11, 626-636.
28. Gu, Y., Arruda-Carvalho, M., Wang, J., Janoschka, S. R., Josselyn, S. A., Frankland, P. W., et al. (2012). Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat. Neurosci. 15, 1700-1706.
29. Guzowski, J. F., Miyashita, T., Chawla, M. K., Sanderson, J., Maes, L. I., Houston, F. P., et al. (2006). Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc. Natl. Acad. Sci. U.S.A. 103, 1077-1082.
30. Henze, D. A., Wittner, L., and Buzsaki, G. (2002). Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 5, 790-795.
31. Hjorth-Simonsen, A. (1972). Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. Comp. Neurol. 146, 219-232.
32. Hjorth-Simonsen, A., and Jeune, B. (1972). Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144, 215-232.
33. Ide, Y., Fujiyama, F., Okamoto-Furuta, K., Tamamaki, N., Kaneko, T., and Hisatsune, T. (2008). Rapid integration of young newborn dentate gyrus granule cells in the adult hippocampal circuitry. Eur. J. Neurosci. 28, 2381-2392.
34. Inokuchi, K. (2011). Adult neurogenesis and modulation of neural circuit function. Curr. Opin. Neurobiol. 21, 360-364.
35. Jensen, O., Kaiser, J., and Lachaux, J. P. (2007). Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 30, 317-324.
36. Jung, M. W., and McNaughton, B. L. (1993). Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3, 165-182.
37. Kaplan, M. S., and Hinds, J. W. (1977). Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197, 1092-1094.
38. Karten, Y. J., Jones, M. A., Jeurling, S. I., and Cameron, H. A. (2006). GABAergic signaling in young granule cells in the adult rat and mouse dentate gyrus. Hippocampus 16, 312-320.
39. Kerr, K. M., Agster, K. L., Furtak, S. C., and Burwell, R. D. (2007). Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 17, 697-708.
40. Kesner, R. P. (2013). An analysis of the dentate gyrus function. Behav. Brain Res. doi: 10.1016/j.bbr.2013.01.012. [Epub ahead of print].
41. Kheirbek, M. A., Tannenholz, L., and Hen, R. (2012). NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J. Neurosci. 32, 8696-8702.
42. Kim, W. R., Christian, K., Ming, G. L., and Song, H. (2012). Time-dependent involvement of adult-born dentate granule cells in behavior. Behav. Brain Res. 227, 470-479.
43. Korotkova, T., Fuchs, E. C., Ponomarenko, A., Von Engelhardt, J., and Monyer, H. (2010). NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68, 557-569.
44. Kuhn, H. G., Dickinson-Anson, H., and Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033.
45. Lacefield, C. O., Itskov, V., Reardon, T., Hen, R., and Gordon, J. A. (2012). Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 22, 106-116.
46. Laplagne, D. A., Esposito, M. S., Piatti, V. C., Morgenstern, N. A., Zhao, C., Van Praag, H., et al. (2006). Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol. 4:e409. doi: 10.1371/journal.pbio.0040409
47. Laplagne, D. A., Kamienkowski, J. E., Esposito, M. S., Piatti, V. C., Zhao, C., Gage, F. H., et al. (2007). Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur. J. Neurosci. 25, 2973-2981.
48. Leutgeb, J. K., Leutgeb, S., Moser, M. B., and Moser, E. I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966.
49. Lisman, J. (2010). Working memory: the importance of theta and gamma oscillations. Curr. Biol. 20, R490-R492.
50. Luu, P., Sill, O. C., Gao, L., Becker, S., Wojtowicz, J. M., and Smith, D. M. (2012). The role of adult hippocampal neurogenesis in reducing interference. Behav. Neurosci. 126, 381-391.
51. Ma, D. K., Kim, W. R., Ming, G. L., and Song, H. (2009). Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann. N.Y. Acad. Sci. 1170, 664-673.
52. Manns, J. R., and Eichenbaum, H. (2006). Evolution of declarative memory. Hippocampus 16, 795-808.
53. Marin-Burgin, A., Mongiat, L. A., Pardi, M. B., and Schinder, A. F. (2012). Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335, 1238-1242.
54. Marin-Burgin, A., and Schinder, A. F. (2012). Requirement of adult-born neurons for hippocampus-dependent learning. Behav. Brain Res. 227, 391-399.
55. McNaughton, B. L., and Morris, R. G. M. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10, 408-415.
56. Ming, G. L., and Song, H. (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687-702.
57. Miyashita, T., Kubik, S., Haghighi, N., Steward, O., and Guzowski, J. F. (2009). Rapid activation of plasticity-associated gene transcription in hippocampal neurons provides a mechanism for encoding of one-trial experience. J. Neurosci. 29, 898-906.
58. Mongiat, L. A., Esposito, M. S., Lombardi, G., and Schinder, A. F. (2009). Reliable activation of immature neurons in the adult hippocampus. PLoS ONE 4:e5320. doi: 10.1371/journal.pone.0005320
59. Mongiat, L. A., and Schinder, A. F. (2011). Adult neurogenesis and the plasticity of the dentate gyrus network. Eur. J. Neurosci. 33, 1055-1061.
60. Morris, A. M., Churchwell, J. C., Kesner, R. P., and Gilbert, P. E. (2012). Selective lesions of the dentate gyrus produce disruptions in place learning for adjacent spatial locations. Neurobiol. Learn. Mem. 97, 326-331.
61. Myers, C. E., and Scharfman, H. E. (2009). A role for hilar cells in pattern separation in the dentate gyrus: a computational approach. Hippocampus 19, 321-337.
62. Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., et al. (2012). Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149, 188-201.
63. Neunuebel, J. P., and Knierim, J. J. (2012). Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J. Neurosci. 32, 3848-3858.
64. Nogues, X., Corsini, M. M., Marighetto, A., and Abrous, D. N. (2012). Functions for adult neurogenesis in memory: an introduction to the neurocomputational approach and to its contribution. Behav. Brain Res. 227, 418-425.
65. O'Reilly, R. C., and McClelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4, 661-682.
66. Piatti, V. C., Davies-Sala, M. G., Esposito, M. S., Mongiat, L. A., Trinchero, M. F., and Schinder, A. F. (2011). The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J. Neurosci. 31, 7715-7728.
67. Piatti, V. C., Esposito, M. S., and Schinder, A. F. (2006). The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist 12, 463-468.
68. Pouille, F., and Scanziani, M. (2001). Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159-1163.
69. Ranck, J. B. Jr., (1973). Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp. Neurol. 41, 461-531.
70. Restivo, L., Josselyn, S. A., and Frankland, P. W. (2012). "Functional and anatomical connectivity with CA3 inhibitory interneurons underlies integration of newborn dentate granule cells into the adult hippocampus," in Program No. 290.05. 2012 Neuroscience Meeting Planner (New Orleans, LA: Society for Neuroscience) [Online].
71. Rolls, E. T. (1990). Theoretical and neurophysiological analysis of the functions of the primate hippocampus in memory. Cold Spring Harb. Symp. Quant. Biol. 55, 995-1006.
72. Rolls, E. T. (2010). A computational theory of episodic memory formation in the hippocampus. Behav. Brain Res. 215, 180-196.
73. Ruediger, S., Vittori, C., Bednarek, E., Genoud, C., Strata, P., Sacchetti, B., et al. (2011). Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473, 514-518.
74. Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., et al. (2011a). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470.
75. Sahay, A., Wilson, D. A., and Hen, R. (2011b). Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70, 582-588.
76. Saxe, M. D., Malleret, G., Vronskaya, S., Mendez, I., Garcia, A. D., Sofroniew, M. V., et al. (2007). Paradoxical influence of hippocampal neurogenesis on working memory. Proc. Natl. Acad. Sci. U.S.A. 104, 4642-4646.
77. Scharfman, H. E. (1991). Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J. Neurosci. 11, 1660-1673.
78. Scharfman, H. E. (1995). Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J. Neurophysiol. 74, 179-194.
79. Scharfman, H. E. (2007). The CA3 "backprojection" to the dentate gyrus. Prog. Brain Res. 163, 627-637.
80. Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184-187.
81. Schwartzkroin, P. A., Scharfman, H. E., and Sloviter, R. S. (1990). Similarities in circuitry between Ammon's horn and dentate gyrus: local interactions and parallel processing. Prog. Brain Res. 83, 269-286.
82. Singer, B. H., Gamelli, A. E., Fuller, C. L., Temme, S. J., Parent, J. M., and Murphy, G. G. (2011). Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice. Proc. Natl. Acad. Sci. U.S.A. 108, 5437-5442.
83. Snyder, J. S., Kee, N., and Wojtowicz, J. M. (2001). Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85, 2423-2431.
84. Song, J., Christian, K. M., Ming, G. L., and Song, H. (2012). Modification of hippocampal circuitry by adult neurogenesis. Dev. Neurobiol. 72, 1032-1043.
85. Steward, O., and Scoville, S. A. (1976). Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169, 347-370.
86. Stocca, G., Schmidt-Hieber, C., and Bischofberger, J. (2008). Differential dendritic Ca2+ signalling in young and mature hippocampal granule cells. J. Physiol. 586, 3795-3811.
87. Stone, S. S., Teixeira, C. M., Zaslavsky, K., Wheeler, A. L., Martinez-Canabal, A., Wang, A. H., et al. (2011). Functional convergence of developmentally and adult-generated granule cells in dentate gyrus circuits supporting hippocampus-dependent memory. Hippocampus 21, 1348-1362.
88. Tashiro, A., Makino, H., and Gage, F. H. (2007). Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci. 27, 3252-3259.
89. Tashiro, A., Sandler, V. M., Toni, N., Zhao, C., and Gage, F. H. (2006). NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442, 929-933.
90. Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., et al. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11, 901-907.
91. Toni, N., Teng, E. M., Bushong, E. A., Aimone, J. B., Zhao, C., Consiglio, A., et al. (2007). Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci. 10, 727-734.
92. Treves, A., and Rolls, E. T. (1992). Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2, 189-199.
93. Treves, A., and Rolls, E. T. (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374-391.
94. Tronel, S., Belnoue, L., Grosjean, N., Revest, J. M., Piazza, P. V., Koehl, M., et al. (2012). Adult-born neurons are necessary for extended contextual discrimination. Hippocampus 22, 292-298.
95. Trouche, S., Bontempi, B., Roullet, P., and Rampon, C. (2009). Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory. Proc. Natl. Acad. Sci. U.S.A. 106, 5919-5924.
96. Van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034.
97. Vivar, C., Potter, M. C., Choi, J., Lee, J. Y., Stringer, T. P., Callaway, E. M., et al. (2012). Monosynaptic inputs to new neurons in the dentate gyrus. Nat. Commun. 3:1107. doi: 10.1038/ncomms2101
98. Wang, L. P., Kempermann, G., and Kettenmann, H. (2005). A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol. Cell. Neurosci. 29, 181-189.
99. Warner-Schmidt, J. L., and Duman, R. S. (2006). Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16, 239-249.
100. West, M. J., Slomianka, L., and Gundersen, H. J. (1991). Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482-497.
101. Wilson, M. A., and McNaughton, B. L. (1993). Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058.
102. Winocur, G., Becker, S., Luu, P., Rosenzweig, S., and Wojtowicz, J. M. (2012). Adult hippocampal neurogenesis and memory interference. Behav. Brain Res. 227, 464-469.
103. Witter, M. P. (2007). The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog. Brain Res. 163, 43-61.
104. Witter, M. P., and Amaral, D. G. (1991). Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J. Comp. Neurol. 307, 437-459.
105. Witter, M. P., Groenewegen, H. J., Lopes Da Silva, F. H., and Lohman, A. H. (1989). Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33, 161-253.
106. Xu, Z., Li, J., Zhang, F., Wu, Y., Gao, Y., Liang, J., et al. (2011). Working memory task decreases the survival of newly born neurons in hippocampus. Neurobiol. Learn. Mem. 95, 239-247.
107. Ylinen, A., Bragin, A., Nadasdy, Z., Jando, G., Szabo, I., Sik, A., et al. (1995a). Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30-46.
108. Ylinen, A., Soltesz, I., Bragin, A., Penttonen, M., Sik, A., and Buzsaki, G. (1995b). Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5, 78-90.
109. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660.
110. Zhao, C., Teng, E. M., Summers, R. G. Jr., Ming, G. L., and Gage, F. H. (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26, 3-11.