Distinct hippocampal time cell sequences represent odor memories in immobilized rats

Journal of Neuroscience

Volumn 33, Issue 36, 2013, Pages 14607-14616

  MacDonald, Christopher J ^a   Carrow, Stephen ^a   Place, Ryan ^a   Eichenbaum, Howard ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; LONG EVANS RAT; MALE; NONHUMAN; ODOR; PRIORITY JOURNAL; RAT; SENSORY MEMORY; SENSORY STIMULATION; SPIKE WAVE; STIMULUS RESPONSE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; HEAD; HEAD MOVEMENTS; MALE; MEMORY; NEURONS; ODORS; RATS; RATS, LONG-EVANS; RESTRAINT, PHYSICAL; SMELL; TIME FACTORS;

EID: 84883361402     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1537-13.2013     Document Type: Article

References (43)

1. Allen K, Rawlins JN, BannermanDM, Csicsvari J (2012) Hippocampal place cells can encode multiple trial-dependent features through rate remapping. J Neurosci 32:14752-14766. CrossRef Medline
2. Berens P (2009) CircStat: a Matlab toolbox for circular statistics. J Statistical Software 31:Issue 10.
3. Bland BH (1986) The physiology and pharmacology of hippocampal formation θ rhythms. Prog Neurobiol 26:1-54. CrossRef Medline
4. Buzsáki G (2005) Theta rhythm of navigation: link between path integration and lang mark navigation, episodic and semantic memory. Hippocampus 15:827-840. CrossRef Medline
5. Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139-171. Medline
6. Carr MF, Jadhav SP, Frank LM (2011) Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci 14:147-153. CrossRef Medline
7. Chen G, King JA, Burgess N, O'Keefe J (2013) How vision and movement combine in the hippocampal place code. Proc Natl Acad Sci U S A 110: 378-383. CrossRef Medline
8. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274-287. Medline
9. Dragoi G, Tonegawa S (2011) Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469:397-401. CrossRef Medline
10. Foster TC, Castro CA, McNaughton BL (1989) Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science 244:1580-1582. CrossRef Medline
11. Fox SE, Ranck JB Jr (1981) Electrophysiological characteristics of hippocampal complex-spiking and θ cells. Exp Brain Res 41:399-410. Medline
12. Fox SE, Wolfson S, Ranck JB Jr (1986) Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62:495-508. Medline
13. Gill PR, Mizumori SJ, Smith DM (2011) Hippocampal episode fields develop with learning. Hippocampus 21:1240-1249. CrossRef Medline
14. Harvey CD, Collman F, Dombeck DA, Tank DW (2009) Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461: 941-946. CrossRef Medline
15. Hasselmo ME, Bodelón C, Wyble BP (2002) A proposed function for hippocampal θ rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Computation 14:793-817. CrossRef Medline
16. Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T (2009) Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12:1586-1593. CrossRef Medline
17. Itskov PM, Vinnik E, Diamond ME (2011) Hippocampal representation of touch-guided behavior in rats: persistent and independent traces of stimulus and reward location. PLoS One 6:e16462. CrossRef Medline
18. Jezek K, Henriksen EJ, Treves A, Moser EI, Moser MB (2011) θ-paced flickering between place-cell maps in the hippocampus. Nature 478:246-249. CrossRef Medline
19. Kraus BJ, Robinson RJ 2nd, White JA, Eichenbaum H, Hasselmo ME (2013) Hippocampal "time cells": time versus path integration. Neuron 78:1-12. CrossRef Medline
20. Lenck-Santini PP, Fenton AA, Muller RU (2008) Discharge properties of hippocampal neurons during performance of a jump avoidance task. J Neurosci 28:6773-6786. CrossRef Medline
21. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305: 1295-1298. CrossRef Medline
22. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619-623. CrossRef Medline
23. Lu XC, Slotnick BM, SilberbergAM (1993) Odor matching and odor memory in the rat. Physiol Behav 53:795-804. CrossRef Medline
24. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H (2011) Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 71:737-749. CrossRef Medline
25. Manns JR, Howard MW, Eichenbaum H (2007) Gradual changes in hippocampal activity support remember the order of events. Neuron 26: 530-540. CrossRef Medline
26. Markus EJ, Barnes CL, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4:410-421. Medline
27. McCullagh P, Nelder JA (1989) Generalized linear models. Boca Raton, FL: Chapman and Hall/CRC.
28. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the 'cognitive map.' Nat Rev Neurosci 7:663-678. CrossRef Medline
29. Mitra P, Bokil H (2008) Observed brain dynamics. New York: Oxford UP.
30. Mizuseki K, Sirota A, Pastalkova E, Buzsáki G (2009) θ oscillations provide temporal windows for local circuit computation in the entorhinalhippocampal loop. Neuron 64:267-280. CrossRef Medline
31. Moita AP, Rosis S, Zhou Y, LeDoux JE, Blair HT (2003) Hippocampal place cells acquire location-specific response to the conditioned stimulus during auditory fear conditioning. Neuron 37:485-497. CrossRef Medline
32. Naya Y, Suzuki WA (2011) Integrating what and when across the primate medial temporal lobe. Science 333:773-776. CrossRef Medline
33. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322-1327. CrossRef Medline
34. Robitsek JR, White J, Eichenbaum H (2013) Place cell activation predicts subsequent memory. Behav Brain Res Advance online publication. doi: 10.1016/j.bbr.2012.12.034. CrossRef
35. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsáki G (2012) Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15:769-775. CrossRef Medline
36. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ (1993) An information-theoretic approach to deciphering the hippocampal code. Neural Inf Process Syst 5:1030-1037.
37. Song EY, Kim YB, Kim YH, Jung MW (2005) Role of active movement in place-specific firing of hippocampal neurons. Hippocampus 15:8-17. CrossRef Medline
38. Stapleton JR, Lavine M, Wolpert RL, Nicolelis MA, Simon SA (2006) Rapid taste responses in the gustatory cortex during licking. J Neurosci 26:4126-4138. CrossRef Medline
39. Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, McNaughton BL (2005) Self-motion and the hippocampal spatial metric. J Neurosci 25: 8085-8096. CrossRef Medline
40. Tulving E (1983) Elements of episodic memory. New York: Oxford UP.
41. Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M (1997) Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277:376-380. CrossRef Medline
42. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613-616. CrossRef Medline
43. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623-633. CrossRef Medline