Hippocampal Somatostatin Interneurons Control the Size of Neuronal Memory Ensembles

Neuron

Volumn 89, Issue 5, 2016, Pages 1074-1085

  Stefanelli, Thomas ^a   Bertollini, Cristina ^a   Lüscher, Christian ^a,b   Muller, Dominique ^a   Mendez, Pablo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOSTATIN; CHANNELRHODOPSIN 2, MOUSE; PARVALBUMIN; PHOTOPROTEIN; RHODOPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SIZE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; GRANULE CELL; INTERNEURON; MEMORY; MOUSE; NERVE CELL INHIBITION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; SHORT TERM MEMORY; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; CELL COUNT; CELL SIZE; CONDITIONING; CYTOLOGY; FEAR; GENETICS; MAZE TEST; METABOLISM; NONPARAMETRIC TEST; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SPATIAL BEHAVIOR; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; CELL COUNT; CELL SIZE; CONDITIONING (PSYCHOLOGY); DENTATE GYRUS; FEAR; INTERNEURONS; LUMINESCENT PROTEINS; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RHODOPSIN; SOMATOSTATIN; SPATIAL BEHAVIOR; STATISTICS, NONPARAMETRIC;

EID: 84960336195     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.01.024     Document Type: Article

References (53)

1. Acsády L., Kamondi A., Sík A., Freund T., Buzsáki G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 1998, 18:3386-3403.
2. Berger T.K., Silberberg G., Perin R., Markram H. Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol. 2010, 8:e1000473.
3. Chalifoux J.R., Carter A.G. GABAB receptors modulate NMDA receptor calcium signals in dendritic spines. Neuron 2010, 66:101-113.
4. Chiu C.Q., Lur G., Morse T.M., Carnevale N.T., Ellis-Davies G.C., Higley M.J. Compartmentalization of GABAergic inhibition by dendritic spines. Science 2013, 340:759-762.
5. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De Felipe J., Ben-Ari Y., Esclapez M., Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 2001, 4:52-62.
6. Cowansage K.K., Shuman T., Dillingham B.C., Chang A., Golshani P., Mayford M. Direct reactivation of a coherent neocortical memory of context. Neuron 2014, 84:432-441.
7. Deng W., Mayford M., Gage F.H. Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. eLife 2013, 2:e00312.
8. Denny C.A., Kheirbek M.A., Alba E.L., Tanaka K.F., Brachman R.A., Laughman K.B., Tomm N.K., Turi G.F., Losonczy A., Hen R. Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis. Neuron 2014, 83:189-201.
9. Donato F., Rompani S.B., Caroni P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 2013, 504:272-276.
10. Frankland P.W., O'Brien C., Ohno M., Kirkwood A., Silva A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 2001, 411:309-313.
11. Freund T.F., Katona I. Perisomatic inhibition. Neuron 2007, 56:33-42.
12. Goold C.P., Nicoll R.A. Single-cell optogenetic excitation drives homeostatic synaptic depression. Neuron 2010, 68:512-528.
13. Han J.H., Kushner S.A., Yiu A.P., Cole C.J., Matynia A., Brown R.A., Neve R.L., Guzowski J.F., Silva A.J., Josselyn S.A. Neuronal competition and selection during memory formation. Science 2007, 316:457-460.
14. Han J.H., Kushner S.A., Yiu A.P., Hsiang H.L., Buch T., Waisman A., Bontempi B., Neve R.L., Frankland P.W., Josselyn S.A. Selective erasure of a fear memory. Science 2009, 323:1492-1496.
15. 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.
16. Katona L., Lapray D., Viney T.J., Oulhaj A., Borhegyi Z., Micklem B.R., Klausberger T., Somogyi P. Sleep and movement differentiates actions of two types of somatostatin-expressing GABAergic interneuron in rat hippocampus. Neuron 2014, 82:872-886.
17. Kawashima T., Okuno H., Nonaka M., Adachi-Morishima A., Kyo N., Okamura M., Takemoto-Kimura S., Worley P.F., Bito H. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc. Natl. Acad. Sci. USA 2009, 106:316-321.
18. Kheirbek M.A., Drew L.J., Burghardt N.S., Costantini D.O., Tannenholz L., Ahmari S.E., Zeng H., Fenton A.A., Hen R. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 2013, 77:955-968.
19. Krueppel R., Remy S., Beck H. Dendritic integration in hippocampal dentate granule cells. Neuron 2011, 71:512-528.
20. Lewis D.A., Hashimoto T., Volk D.W. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 2005, 6:312-324.
21. 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.
22. Lovett-Barron M., Kaifosh P., Kheirbek M.A., Danielson N., Zaremba J.D., Reardon T.R., Turi G.F., Hen R., Zemelman B.V., Losonczy A. Dendritic inhibition in the hippocampus supports fear learning. Science 2014, 343:857-863.
23. Maccaferri G. Stratum oriens horizontal interneurone diversity and hippocampal network dynamics. J. Physiol. 2005, 562:73-80.
24. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
25. Maren S., Quirk G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 2004, 5:844-852.
26. Marín O. Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 2012, 13:107-120.
27. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
28. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 2000, 23:649-711.
29. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
30. McHugh T.J., Tonegawa S. Spatial exploration is required for the formation of contextual fear memory. Behav. Neurosci. 2007, 121:335-339.
31. Mendez P., Bacci A. Assortment of GABAergic plasticity in the cortical interneuron melting pot. Neural. Plast. 2011, 10.1155/2011/976856.
32. Miles R., Tóth K., Gulyás A.I., Hájos N., Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 1996, 16:815-823.
33. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 1991, 14:421-451.
34. Nabavi S., Fox R., Proulx C.D., Lin J.Y., Tsien R.Y., Malinow R. Engineering a memory with LTD and LTP. Nature 2014, 511:348-352.
35. Olshausen B.A., Field D.J. Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 2004, 14:481-487.
36. Pierson J.L., Pullins S.E., Quinn J.J. Dorsal hippocampus infusions of CNQX into the dentate gyrus disrupt expression of trace fear conditioning. Hippocampus 2015, 25:779-785.
37. Ramirez S., Liu X., Lin P.A., Suh J., Pignatelli M., Redondo R.L., Ryan T.J., Tonegawa S. Creating a false memory in the hippocampus. Science 2013, 341:387-391.
38. Reijmers L.G., Perkins B.L., Matsuo N., Mayford M. Localization of a stable neural correlate of associative memory. Science 2007, 317:1230-1233.
39. Rogerson T., Cai D.J., Frank A., Sano Y., Shobe J., Lopez-Aranda M.F., Silva A.J. Synaptic tagging during memory allocation. Nat. Rev. Neurosci. 2014, 15:157-169.
40. Schmidt B., Marrone D.F., Markus E.J. Disambiguating the similar: the dentate gyrus and pattern separation. Behav. Brain Res. 2012, 226:56-65.
41. Silberberg G., Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 2007, 53:735-746.
42. Smeyne R.J., Schilling K., Robertson L., Luk D., Oberdick J., Curran T., Morgan J.I. fos-lacZ transgenic mice: mapping sites of gene induction in the central nervous system. Neuron 1992, 8:13-23.
43. Sparta D.R., Stamatakis A.M., Phillips J.L., Hovelsø N., van Zessen R., Stuber G.D. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat. Protoc. 2012, 7:12-23.
44. 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.
45. Tanaka K.Z., Pevzner A., Hamidi A.B., Nakazawa Y., Graham J., Wiltgen B.J. Cortical representations are reinstated by the hippocampus during memory retrieval. Neuron 2014, 84:347-354.
46. Tashiro A., Makino H., Gage F.H. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci. 2007, 27:3252-3259.
47. Tayler K.K., Tanaka K.Z., Reijmers L.G., Wiltgen B.J. Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr. Biol. 2013, 23:99-106.
48. Treves A., Rolls E.T. Computational analysis of the role of the hippocampus in memory. Hippocampus 1994, 4:374-391.
49. Urban-Ciecko J., Fanselow E.E., Barth A.L. Neocortical somatostatin neurons reversibly silence excitatory transmission via GABAb receptors. Curr. Biol. 2015, 25:722-731.
50. Verret L., Mann E.O., Hang G.B., Barth A.M., Cobos I., Ho K., Devidze N., Masliah E., Kreitzer A.C., Mody I., et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012, 149:708-721.
51. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
52. 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.
53. Yiu A.P., Mercaldo V., Yan C., Richards B., Rashid A.J., Hsiang H.L., Pressey J., Mahadevan V., Tran M.M., Kushner S.A., et al. Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 2014, 83:722-735.