Entorhinal Cortical Ocean Cells Encode Specific Contexts and Drive Context-Specific Fear Memory

Neuron

Volumn 87, Issue 6, 2015, Pages 1317-1331

  Kitamura, Takashi ^a   Sun, Chen ^a   Martin, Jared ^a   Kitch, Lacey J ^b   Schnitzer, Mark J ^b,c   Tonegawa, Susumu ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL ACTIVITY; CELL LABELING; CONDITIONING; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; EPISODIC MEMORY; FEAR; HIPPOCAMPAL CA3 REGION; ISLAND CELL; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE PROJECTION; NONHUMAN; OCEAN CELL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; STATE DEPENDENT LEARNING; STELLATE CELL; TEMPORAL LOBE; ANIMAL; C57BL MOUSE; CYTOLOGY; MEMORY; NERVE TRACT; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ENTORHINAL CORTEX; FEAR; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL PATHWAYS;

EID: 84942134704     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.08.036     Document Type: Article

References (51)

1. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 1965, 124:319-335.
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. Bakker A., Kirwan C.B., Miller M., Stark C.E. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319:1640-1642.
4. Canto C.B., Wouterlood F.G., Witter M.P. What does the anatomical organization of the entorhinal cortex tell us?. Neural Plast. 2008, 2008:381243.
5. Chen T.W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
6. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., Jessberger S., Saksida L.M., Barker R.A., Gage F.H., Bussey T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
7. Creer D.J., Romberg C., Saksida L.M., van Praag H., Bussey T.J. Running enhances spatial pattern separation in mice. Proc. Natl. Acad. Sci. USA 2010, 107:2367-2372.
8. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci. 2010, 11:339-350.
9. 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.
10. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 2000, 1:41-50.
11. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
12. Frank L.M., Stanley G.B., Brown E.N. Hippocampal plasticity across multiple days of exposure to novel environments. J. Neurosci. 2004, 24:7681-7689.
13. Ge S., Yang C.H., Hsu K.S., Ming G.L., Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 2007, 54:559-566.
14. Gilbert P.E., Kesner R.P., Lee I. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 2001, 11:626-636.
15. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
16. Kesner R.P., Gilbert P.E., Wallenstein G.V. Testing neural network models of memory with behavioral experiments. Curr. Opin. Neurobiol. 2000, 10:260-265.
17. Kheirbek M.A., Tannenholz L., Hen R. NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J. Neurosci. 2012, 32:8696-8702.
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. Kitamura T., Saitoh Y., Takashima N., Murayama A., Niibori Y., Ageta H., Sekiguchi M., Sugiyama H., Inokuchi K. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009, 139:814-827.
20. Kitamura T., Pignatelli M., Suh J., Kohara K., Yoshiki A., Abe K., Tonegawa S. Island cells control temporal association memory. Science 2014, 343:896-901.
21. Kohara K., Pignatelli M., Rivest A.J., Jung H.Y., Kitamura T., Suh J., Frank D., Kajikawa K., Mise N., Obata Y., et al. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat. Neurosci. 2014, 17:269-279.
22. Leutgeb S., Leutgeb J.K., Treves A., Moser M.B., Moser E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 2004, 305:1295-1298.
23. 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.
24. 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.
25. Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1971, 262:23-81.
26. Mattis J., Tye K.M., Ferenczi E.A., Ramakrishnan C., O'Shea D.J., Prakash R., Gunaydin L.A., Hyun M., Fenno L.E., Gradinaru V., et al. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 2012, 9:159-172.
27. 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.
28. 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.
29. Niibori Y., Yu T.S., Epp J.R., Akers K.G., Josselyn S.A., Frankland P.W. Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region. Nat. Commun. 2012, 3:1253.
30. O'Reilly R.C., McClelland J.L. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 1994, 4:661-682.
31. 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.
32. Ray S., Naumann R., Burgalossi A., Tang Q., Schmidt H., Brecht M. Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science 2014, 343:891-896.
33. Reijmers L.G., Perkins B.L., Matsuo N., Mayford M. Localization of a stable neural correlate of associative memory. Science 2007, 317:1230-1233.
34. 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.
35. Sahay A., Scobie K.N., Hill A.S., O'Carroll C.M., Kheirbek M.A., Burghardt N.S., Fenton A.A., Dranovsky A., Hen R. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011, 472:466-470.
36. Sariñana J., Kitamura T., Künzler P., Sultzman L., Tonegawa S. Differential roles of the dopamine 1-class receptors, D1R and D5R, in hippocampal dependent memory. Proc. Natl. Acad. Sci. USA 2014, 111:8245-8250.
37. Schlessinger A.R., Cowan W.M., Gottlieb D.I. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 1975, 159:149-175.
38. Schmidt-Hieber C., Jonas P., Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004, 429:184-187.
39. Scobie K.N., Hall B.J., Wilke S.A., Klemenhagen K.C., Fujii-Kuriyama Y., Ghosh A., Hen R., Sahay A. Krüppel-like factor 9 is necessary for late-phase neuronal maturation in the developing dentate gyrus and during adult hippocampal neurogenesis. J. Neurosci. 2009, 29:9875-9887.
40. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 1957, 20:11-21.
41. Seki T., Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci. 1993, 13:2351-2358.
42. Steward O. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comp. Neurol. 1976, 167:285-314.
43. 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.
44. Sun C., Kitamura T., Yamamoto J., Martin J., Pignatelli M., Kitch L.J., Schnitzer M.J., Tonegawa S. Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells. Proc. Natl. Acad. Sci. USA 2015, 112:9466-9471.
45. Treves A., Rolls E.T. Computational analysis of the role of the hippocampus in memory. Hippocampus 1994, 4:374-391.
46. Tulving E. Episodic memory: from mind to brain. Annu. Rev. Psychol. 2002, 53:1-25.
47. Varga C., Lee S.Y., Soltesz I. Target-selective GABAergic control of entorhinal cortex output. Nat. Neurosci. 2010, 13:822-824.
48. Wintzer M.E., Boehringer R., Polygalov D., McHugh T.J. The hippocampal CA2 ensemble is sensitive to contextual change. J. Neurosci. 2014, 34:3056-3066.
49. Witter M.P., Wouterlood F.G., Naber P.A., Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Ann. N Y Acad. Sci. 2000, 911:1-24.
50. 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.
51. Ziv Y., Burns L.D., Cocker E.D., Hamel E.O., Ghosh K.K., Kitch L.J., El Gamal A., Schnitzer M.J. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 2013, 16:264-266.