A Cortico-Hippocampal Learning Rule Shapes Inhibitory Microcircuit Activity to Enhance Hippocampal Information Flow

Neuron

Volumn 79, Issue 6, 2013, Pages 1208-1221

  Basu, Jayeeta ^a   Srinivas, KalyanV ^a   Cheung, StephanieK ^a   Taniguchi, Hiroki ^b,c   Huang, Z Josh ^b   Siegelbaum, StevenA ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; ENTORHINAL CORTEX; FEEDFORWARD INHIBITION; HIPPOCAMPAL CA1 REGION; INFORMATION PROCESSING; INPUT TIMING DEPENDENT PLASTICITY; INTERNEURON; LONG TERM DEPRESSION; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; OPTOGENETICS; PHARMACOGENETICS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; BIOPHYSICS; CALCIUM; CEREBRAL CORTEX; CHOLECYSTOKININ; COMPUTER SIMULATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; INHIBITORY POSTSYNAPTIC POTENTIALS; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; NERVE NET; NEURAL PATHWAYS; NEURONS; OPTOGENETICS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RHODOPSIN; SYNAPSES;

EID: 84884253993     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.001     Document Type: Article

References (58)

1. Abbott L.F., Regehr W.G. Synaptic computation. Nature 2004, 431:796-803.
2. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989, 31:571-591.
3. Bender V.A., Bender K.J., Brasier D.J., Feldman D.E. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J.Neurosci. 2006, 26:4166-4177.
4. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
5. Brenowitz S.D., Regehr W.G. Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 2005, 45:419-431.
6. Buzsáki G. Feed-forward inhibition in the hippocampal formation. Prog. Neurobiol. 1984, 22:131-153.
7. Buzsáki G. Neural syntax: cell assemblies, synapsembles, and readers. Neuron 2010, 68:362-385.
8. Buzsáki G., Wang X.J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 2012, 35:203-225.
9. Castillo P.E., Younts T.J., Chávez A.E., Hashimotodani Y. Endocannabinoid signaling and synaptic function. Neuron 2012, 76:70-81.
10. Chevaleyre V., Castillo P.E. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 2003, 38:461-472.
11. Cho J.H., Bayazitov I.T., Meloni E.G., Myers K.M., Carlezon W.A., Zakharenko S.S., Bolshakov V.Y. Coactivation of thalamic and cortical pathways induces input timing-dependent plasticity in amygdala. Nat. Neurosci. 2012, 15:113-122.
12. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J.Neurosci. 1999, 19:274-287.
13. Daw M.I., Tricoire L., Erdelyi F., Szabo G., McBain C.J. Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J.Neurosci. 2009, 29:11112-11122.
14. Dobrunz L.E., Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 1997, 18:995-1008.
15. Dudman J.T., Tsay D., Siegelbaum S.A. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron 2007, 56:866-879.
16. Feldman D.E. The spike-timing dependence of plasticity. Neuron 2012, 75:556-571.
17. Frank L.M., Brown E.N., Wilson M.A. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J.Neurophysiol. 2001, 86:2029-2040.
18. Freund T.F., Katona I. Perisomatic inhibition. Neuron 2007, 56:33-42.
19. Glickfeld L.L., Scanziani M. Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat. Neurosci. 2006, 9:807-815.
20. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
21. Han E.B., Heinemann S.F. Distal dendritic inputs control neuronal activity by heterosynaptic potentiation of proximal inputs. J.Neurosci. 2013, 33:1314-1325.
22. Hefft S., Jonas P. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat. Neurosci. 2005, 8:1319-1328.
23. Hines M.L., Carnevale N.T. The NEURON simulation environment. Neural Comput. 1997, 9:1179-1209.
24. Hippenmeyer S., Vrieseling E., Sigrist M., Portmann T., Laengle C., Ladle D.R., Arber S. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 2005, 3:e159.
25. Isaacson J.S., Scanziani M. How inhibition shapes cortical activity. Neuron 2011, 72:231-243.
26. Ito M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol. Rev. 2001, 81:1143-1195.
27. Jarsky T., Roxin A., Kath W.L., Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2005, 8:1667-1676.
28. Kajiwara R., Wouterlood F.G., Sah A., Boekel A.J., Baks-te Bulte L.T., Witter M.P. Convergence of entorhinal and CA3 inputs onto pyramidal neurons and interneurons in hippocampal area CA1-an anatomical study in the rat. Hippocampus 2008, 18:266-280.
29. Katona I., Sperlágh B., Sík A., Käfalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J.Neurosci. 1999, 19:4544-4558.
30. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
31. Klausberger T., Marton L.F., O'Neill J., Huck J.H., Dalezios Y., Fuentealba P., Suen W.Y., Papp E., Kaneko T., Watanabe M., et al. Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J.Neurosci. 2005, 25:9782-9793.
32. Kullmann D.M., Moreau A.W., Bakiri Y., Nicholson E. Plasticity of inhibition. Neuron 2012, 75:951-962.
33. Levy W.B., Desmond N.L., Zhang D.X. Perforant path activation modulates the induction of long-term potentiation of the schaffer collateral-hippocampal CA1 response: theoretical and experimental analyses. Learn. Mem. 1998, 4:510-518.
34. Losonczy A., Biro A.A., Nusser Z. Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. Proc. Natl. Acad. Sci. USA 2004, 101:1362-1367.
35. Lovett-Barron M., Turi G.F., Kaifosh P., Lee P.H., Bolze F., Sun X.H., Nicoud J.F., Zemelman B.V., Sternson S.M., Losonczy A. Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 2012, 15:423-430. S1-S3.
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. Magnus C.J., Lee P.H., Atasoy D., Su H.H., Looger L.L., Sternson S.M. Chemical and genetic engineering of selective ion channel-ligand interactions. Science 2011, 333:1292-1296.
38. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
39. Mayford M., Siegelbaum S.A., Kandel E.R. Synapses and memory storage. Cold Spring Harb. Perspect. Biol. 2012, 4:4.
40. Miyoshi G., Hjerling-Leffler J., Karayannis T., Sousa V.H., Butt S.J., Battiste J., Johnson J.E., Machold R.P., Fishell G. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J.Neurosci. 2010, 30:1582-1594.
41. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163.
42. Remondes M., Schuman E.M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 2002, 416:736-740.
43. Remondes M., Schuman E.M. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 2004, 431:699-703.
44. Rial Verde E.M., Zayat L., Etchenique R., Yuste R. Photorelease of GABA with visible light using an inorganic caging group. Front Neural Circuits 2008, 2:2.
45. Safo P., Regehr W.G. Timing dependence of the induction of cerebellar LTD. Neuropharmacology 2008, 54:213-218.
46. Sousa V.H., Miyoshi G., Hjerling-Leffler J., Karayannis T., Fishell G. Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb. Cortex 2009, 19(Suppl 1):i1-i10.
47. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008, 9:206-221.
48. Steffenach H.A., Witter M., Moser M.B., Moser E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 2005, 45:301-313.
49. Suh J., Rivest A.J., Nakashiba T., Tominaga T., Tonegawa S. Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 2011, 334:1415-1420.
50. Takahashi H., Magee J.C. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 2009, 62:102-111.
51. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
52. Wigström H., Gustafsson B. Facilitation of hippocampal long-lasting potentiation by GABA antagonists. Acta Physiol. Scand. 1985, 125:159-172.
53. Wilson R.I., Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 2001, 410:588-592.
54. Wöhrl R., von Haebler D., Heinemann U. Low-frequency stimulation of the direct cortical input to area CA1 induces homosynaptic LTD and heterosynaptic LTP in the rat hippocampal-entorhinal cortex slice preparation. Eur. J. Neurosci. 2007, 25:251-258.
55. Xu J.Y., Zhang J., Chen C. Long-lasting potentiation of hippocampal synaptic transmission by direct cortical input is mediated via endocannabinoids. J.Physiol. 2012, 590:2305-2315.
56. Yamamoto M., Shook N.A., Kanisicak O., Yamamoto S., Wosczyna M.N., Camp J.R., Goldhamer D.J. A multifunctional reporter mouse line for Cre- and FLP-dependent lineage analysis. Genesis 2009, 47:107-114.
57. Yeckel M.F., Berger T.W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. Natl. Acad. Sci. USA 1990, 87:5832-5836.
58. Zhang F., Gradinaru V., Adamantidis A.R., Durand R., Airan R.D., de Lecea L., Deisseroth K. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 2010, 5:439-456.