Experience-dependent remodeling of basket cell networks in the dentate gyrus

Neuron

Volumn 84, Issue 1, 2014, Pages 107-122

  Pieraut, Simon ^a   Gounko, Natalia ^a,d   Sando, Richard ^a   Dang, Westley ^a   Rebboah, Elisabeth ^a   Panda, Satchidananda ^b   Madisen, Linda ^c   Zeng, Hongkui ^c   Maximov, Anton ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CALRETININ; GLUTAMIC ACID; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SOMATOSTATIN; SYNAPTOPORIN; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASKET CELL NETWORK; BRAIN CORTEX; CELL ACTIVITY; CELL DENSITY; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPUS; INTERNEURON; MOUSE; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; SYNAPTIC TRANSMISSION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; CELL DIFFERENTIATION; DENTATE GYRUS; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE NET; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES;

EID: 84908008850     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.09.012     Document Type: Article

References (65)

1. Acsády L., Káli S. Models, structure, function: the transformation of cortical signals in the dentate gyrus. Prog. Brain Res. 2007, 163:577-599.
2. Adesnik H., Li G., During M.J., Pleasure S.J., Nicoll R.A. NMDA receptors inhibit synapse unsilencing during brain development. Proc. Natl. Acad. Sci. USA 2008, 105:5597-5602.
3. Bagnall M.W., Hull C., Bushong E.A., Ellisman M.H., Scanziani M. Multiple clusters of release sites formed by individual thalamic afferents onto cortical interneurons ensure reliable transmission. Neuron 2011, 71:180-194.
4. 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.
5. Bloodgood B.L., Sharma N., Browne H.A., Trepman A.Z., Greenberg M.E. The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition. Nature 2013, 503:121-125.
6. Bortone D., Polleux F. KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 2009, 62:53-71.
7. Burger C., Gorbatyuk O.S., Velardo M.J., Peden C.S., Williams P., Zolotukhin S., Reier P.J., Mandel R.J., Muzyczka N. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther. 2004, 10:302-317.
8. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Targeted optogenetic stimulation and recording of neurons invivo using cell-type-specific expression of Channelrhodopsin-2. Nat. Protoc. 2010, 5:247-254.
9. Carlén M., Meletis K., Siegle J.H., Cardin J.A., Futai K., Vierling-Claassen D., Rühlmann C., Jones S.R., Deisseroth K., Sheng M., et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol. Psychiatry 2012, 17:537-548.
10. Castillo P.E., Schoch S., Schmitz F., Südhof T.C., Malenka R.C. RIM1alpha is required for presynaptic long-term potentiation. Nature 2002, 415:327-330.
11. Chattopadhyaya B., Di Cristo G., Higashiyama H., Knott G.W., Kuhlman S.J., Welker E., Huang Z.J. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J.Neurosci. 2004, 24:9598-9611.
12. Chattopadhyaya B., Di Cristo G., Wu C.Z., Knott G., Kuhlman S., Fu Y., Palmiter R.D., Huang Z.J. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 2007, 54:889-903.
13. Chen J.L., Lin W.C., Cha J.W., So P.T., Kubota Y., Nedivi E. Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat. Neurosci. 2011, 14:587-594.
14. Chen J.L., Villa K.L., Cha J.W., So P.T., Kubota Y., Nedivi E. Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 2012, 74:361-373.
15. Courchet J., Lewis T.L., Lee S., Courchet V., Liou D.Y., Aizawa S., Polleux F. Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 2013, 153:1510-1525.
16. De Marco García N.V., Karayannis T., Fishell G. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 2011, 472:351-355.
17. DeFelipe J., López-Cruz P.L., Benavides-Piccione R., Bielza C., Larrañaga P., Anderson S., Burkhalter A., Cauli B., Fairén A., Feldmeyer D., et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 2013, 14:202-216.
18. Donato F., Rompani S.B., Caroni P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 2013, 504:272-276.
19. Fishell G., Rudy B. Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu. Rev. Neurosci. 2011, 34:535-567.
20. Flandin P., Zhao Y., Vogt D., Jeong J., Long J., Potter G., Westphal H., Rubenstein J.L. Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors. Neuron 2011, 70:939-950.
21. Förster E., Zhao S., Frotscher M. Laminating the hippocampus. Nat. Rev. Neurosci. 2006, 7:259-267.
22. Galimberti I., Bednarek E., Donato F., Caroni P. EphA4 signaling in juveniles establishes topographic specificity of structural plasticity in the hippocampus. Neuron 2010, 65:627-642.
23. Gittis A.H., Nelson A.B., Thwin M.T., Palop J.J., Kreitzer A.C. Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J.Neurosci. 2010, 30:2223-2234.
24. Harris J.A., Hirokawa K.E., Sorensen S.A., Gu H., Mills M., Ng L.L., Bohn P., Mortrud M., Ouellette B., Kidney J., et al. Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation. Front. Neural Circuits. 2014, 8:76.
25. Hosp J.A., Strüber M., Yanagawa Y., Obata K., Vida I., Jonas P., Bartos M. Morpho-physiological criteria divide dentate gyrus interneurons into classes. Hippocampus 2014, 24:189-203.
26. Houser C.R. Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity. Prog. Brain Res. 2007, 163:217-232.
27. Isaacson J.S., Scanziani M. How inhibition shapes cortical activity. Neuron 2011, 72:231-243.
28. Keck T., Scheuss V., Jacobsen R.I., Wierenga C.J., Eysel U.T., Bonhoeffer T., Hübener M. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 2011, 71:869-882.
29. Kerschensteiner D., Morgan J.L., Parker E.D., Lewis R.M., Wong R.O. Neurotransmission selectively regulates synapse formation in parallel circuits invivo. Nature 2009, 460:1016-1020.
30. Korotkova T., Fuchs E.C., Ponomarenko A., von Engelhardt J., Monyer H. NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 2010, 68:557-569.
31. Kullmann D.M., Moreau A.W., Bakiri Y., Nicholson E. Plasticity of inhibition. Neuron 2012, 75:951-962.
32. Leutgeb J.K., Leutgeb S., Moser M.B., Moser E.I. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 2007, 315:961-966.
33. Lin Y., Bloodgood B.L., Hauser J.L., Lapan A.D., Koon A.C., Kim T.K., Hu L.S., Malik A.N., Greenberg M.E. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 2008, 455:1198-1204.
34. Liu X., Ramirez S., Pang P.T., Puryear C.B., Govindarajan A., Deisseroth K., Tonegawa S. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484:381-385.
35. Lopez C.M., Pelkey K.A., Chittajallu R., Nakashiba T., Toth K., Tonegawa S., McBain C.J. Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus. Front Neural Circuits. 2012, 6:85.
36. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
37. Maffei A., Nelson S.B., Turrigiano G.G. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat. Neurosci. 2004, 7:1353-1359.
38. Matsuda N., Lu H., Fukata Y., Noritake J., Gao H., Mukherjee S., Nemoto T., Fukata M., Poo M.M. Differential activity-dependent secretion of brain-derived neurotrophic factor from axon and dendrite. J.Neurosci. 2009, 29:14185-14198.
39. Maximov A., Tang J., Yang X., Pang Z.P., Südhof T.C. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 2009, 323:516-521.
40. McHugh T.J., Jones M.W., Quinn J.J., Balthasar N., Coppari R., Elmquist J.K., Lowell B.B., Fanselow M.S., Wilson M.A., Tonegawa S. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 2007, 317:94-99.
41. Nakashiba T., Cushman J.D., Pelkey K.A., Renaudineau S., Buhl D.L., McHugh T.J., Rodriguez Barrera V., Chittajallu R., Iwamoto K.S., McBain C.J., et al. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 2012, 149:188-201.
42. Nicoll R.A., Schmitz D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 2005, 6:863-876.
43. O'Sullivan M.L., Martini F., von Daake S., Comoletti D., Ghosh A. LPHN3, a presynaptic adhesion-GPCR implicated in ADHD, regulates the strength of neocortical layer 2/3 synaptic input to layer 5. Neural Dev. 2014, 9:7.
44. Poo C., Isaacson J.S. Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations. Neuron 2009, 62:850-861.
45. Ruediger S., Vittori C., Bednarek E., Genoud C., Strata P., Sacchetti B., Caroni P. Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 2011, 473:514-518.
46. Sambandan S., Sauer J.F., Vida I., Bartos M. Associative plasticity at excitatory synapses facilitates recruitment of fast-spiking interneurons in the dentate gyrus. The Journal of neuroscience 2010, 30:11826-11837.
47. Sando R., Gounko N., Pieraut S., Liao L., Yates J., Maximov A. HDAC4 governs a transcriptional program essential for synaptic plasticity and memory. Cell 2012, 151:821-834.
48. Sando R., Baumgaertel K., Pieraut S., Torabi-Rander N., Wandless T.J., Mayford M., Maximov A. Inducible control of gene expression with destabilized Cre. Nat. Methods 2013, 10:1085-1088.
49. Saura C.A., Choi S.Y., Beglopoulos V., Malkani S., Zhang D., Shankaranarayana Rao B.S., Chattarji S., Kelleher R.J., Kandel E.R., Duff K., et al. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 2004, 42:23-36.
50. Schoch S., Deák F., Königstorfer A., Mozhayeva M., Sara Y., Südhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001, 294:1117-1122.
51. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
52. Spiegel I., Mardinly A.R., Gabel H.W., Bazinet J.E., Couch C.H., Tzeng C.P., Harmin D.A., Greenberg M.E. Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 2014, 157:1216-1229.
53. Taniguchi H., Lu J., Huang Z.J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 2013, 339:70-74.
54. Treves A., Tashiro A., Witter M.P., Moser E.I. What is the mammalian dentate gyrus good for?. Neuroscience 2008, 154:1155-1172.
55. Tricoire L., Pelkey K.A., Erkkila B.E., Jeffries B.W., Yuan X., McBain C.J. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J.Neurosc. 2011, 31:10948-10970.
56. van Groen T., Miettinen P., Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 2003, 13:133-149.
57. van Versendaal D., Rajendran R., Saiepour M.H., Klooster J., Smit-Rigter L., Sommeijer J.P., De Zeeuw C.I., Hofer S.B., Heimel J.A., Levelt C.N. Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 2012, 74:374-383.
58. Wang C.L., Zhang L., Zhou Y., Zhou J., Yang X.J., Duan S.M., Xiong Z.Q., Ding Y.Q. Activity-dependent development of callosal projections in the somatosensory cortex. J.Neurosci. 2007, 27:11334-11342.
59. Wehr M., Zador A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426:442-446.
60. Wilent W.B., Contreras D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat. Neurosci. 2005, 8:1364-1370.
61. Yasuda M., Johnson-Venkatesh E.M., Zhang H., Parent J.M., Sutton M.A., Umemori H. Multiple forms of activity-dependent competition refine hippocampal circuits invivo. Neuron 2011, 70:1128-1142.
62. Yu C.R., Power J., Barnea G., O'Donnell S., Brown H.E., Osborne J., Axel R., Gogos J.A. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 2004, 42:553-566.
63. Zhang L.I., Tan A.Y., Schreiner C.E., Merzenich M.M. Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 2003, 424:201-205.
64. Zhang Y., Narayan S., Geiman E., Lanuza G.M., Velasquez T., Shanks B., Akay T., Dyck J., Pearson K., Gosgnach S., et al. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 2008, 60:84-96.
65. Zipp F., Nitsch R., Soriano E., Frotscher M. Entorhinal fibers form synaptic contacts on parvalbumin-immunoreactive neurons in the rat fascia dentata. Brain Res. 1989, 495:161-166.