Place‐selective firing contributes to the reverse‐order reactivation of CA1 pyramidal cells during sharp waves in open‐field exploration

Abstract

On the linear track, the recent firing sequences of CA1 place cells recur during sharp wave/ripple patterns (SWRs) in a reverse temporal order [Foster & Wilson (2006) Nature , 440 , 680–683]. We have found similar reverse‐order reactivation during SWRs in open‐field exploration where the firing sequence of cells varied before each SWR. Both the onset times and the firing patterns of cells showed a tendency for reversed sequences during SWRs. These effects were observed for SWRs that occurred during exploration, but not for those during longer immobility periods. Additionally, reverse reactivation was stronger when it was preceded by higher speed (> 5 cm/s) run periods. The trend for reverse‐order SWR reactivation was not significantly different in familiar and novel environments, even though SWR‐associated firing rates of both pyramidal cells and interneurons were reduced in novel environments as compared with familiar. During exploration‐associated SWRs (eSWR) place cells retain place‐selective firing [O'Neill et al. (2006) Neuron , 49, 143–155]. Here, we have shown that each cell's firing onset was more delayed and firing probability more reduced during eSWRs the further the rat was from the middle of the cell's place field; that is, cells receiving less momentary place‐related excitatory drive fired later during SWR events. However, even controlling for place field distance, the recent firing of cells was still significantly correlated with SWR reactivation sequences. We therefore propose that both place‐related drive and the firing history of cells contribute to reverse reactivation during eSWRs.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 40

1. 1.

   Behrens CJ, van den Boom LP, de Hoz L, Friedman A, Heinemann U. Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. NatNeurosci. 2005;8:1560-1567.

   Not in our library10.1038/nn1571

2. 2.

   Buzsaki G. Hippocampal sharp waves: their origin and significance. Brain Res. 1986;398:242-252.

   Not in our library10.1016/0006-8993(86)91483-6

3. 3.

   Buzsaki G. Two-stage model of memory trace formation: a role for ‘noisy’ brain states. Neuroscience. 1989;31:551-570.

   Not in our library10.1016/0306-4522(89)90423-5

4. 4.

   Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science. 1992;256:1025-1027.

   Not in our library10.1126/science.1589772

5. 5.

   Buzsaki G, Leung LW, Vanderwolf CH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983;287:139-171.

   Not in our library10.1016/0165-0173(83)90037-1

6. 6.

   Chrobak JJ, Buzsaki G. Selective activation of deep layer (V–VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. JNeurosci. 1994;14:6160-6170.

   Not in our library10.1523/jneurosci.14-10-06160.1994

7. 7.

   Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. JNeurosci. 1999;19:274-287.

   Not in our library10.1523/jneurosci.19-01-00274.1999

8. 8.

   Csicsvari J, Hirase H, Mamiya A, Buzsaki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron. 2000;28:585-594.

   Not in our library10.1016/s0896-6273(00)00135-5

9. 9.

   Czurko A, Hirase H, Csicsvari J, Buzsaki G. Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel. EurJNeurosci. 1999;11:344-352.

   Not in our library10.1046/j.1460-9568.1999.00446.x

10. 10.

    Dragoi G, Buzsaki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron. 2006;50:145-157.

    Not in our library10.1016/j.neuron.2006.02.023

11. 11.

    Ekstrom AD, Meltzer J, McNaughton BL, Barnes CA. NMDA receptor antagonism blocks experience-dependent expansion of hippocampal ‘place fields’. Neuron. 2001;31:631-638.

    Not in our library10.1016/s0896-6273(01)00401-9

12. 12.

    Fenton AA, Muller RU. Place cell discharge is extremely variable during individual passes of the rat through the firing field. ProcNatl AcadSciUSA. 1998;95:3182-3187.

    Not in our library10.1073/pnas.95.6.3182

13. 13.

    Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006;440:680-683.

    Not in our library10.1038/nature04587

14. 14.

    Frank LM, Stanley GB, Brown EN. Hippocampal plasticity across multiple days of exposure to novel environments. JNeurosci. 2004;24:7681-7689.

    Not in our library10.1523/jneurosci.1958-04.2004

15. 15.

    Harris KD, Hirase H, Leinekugel X, Henze DA, Buzsaki G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron. 2001;32:141-149.

    Not in our library10.1016/s0896-6273(01)00447-0

16. 16.

    Hasselmo ME. Neuromodulation: acetylcholine and memory consolidation. Trends CognSci. 1999;3:351-359.

    Not in our library10.1016/s1364-6613(99)01365-0

17. 17.

    Hirase H, Leinekugel X, Czurko A, Csicsvari J, Buzsaki G. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. ProcNatl AcadSciUSA. 2001;98:9386-9390.

    Not in our library10.1073/pnas.161274398

18. 18.

    Huxter J, Burgess N, O'Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature. 2003;425:828-832.

    Not in our library10.1038/nature02058

19. 19.

    Jackson JC, Johnson A, Redish AD. Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. JNeurosci. 2006;26:12415-12426.

    Not in our library10.1523/jneurosci.4118-06.2006

20. 20.

    Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. JNeurosci. 1999;19:4090-4101.

    Not in our library10.1523/jneurosci.19-10-04090.1999

21. 21.

    Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002;36:1183-1194.

    Not in our library10.1016/s0896-6273(02)01096-6

22. 22.

    Louie K, Wilson MA. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001;29:145-156.

    Not in our library10.1016/s0896-6273(01)00186-6

23. 23.

    Maier N, Nimmrich V, Draguhn A. Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. JPhysiol. 2003;550:873-887.

    Not in our library10.1113/jphysiol.2003.044602

24. 24.

    Mehta MR, Barnes CA, McNaughton BL. Experience-dependent, asymmetric expansion of hippocampal place fields. ProcNatl AcadSciUSA. 1997;94:8918-8921.

    Not in our library10.1073/pnas.94.16.8918

25. 25.

    Mehta MR, Quirk MC, Wilson MA. Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron. 2000;25:707-715.

    Not in our library10.1016/s0896-6273(00)81072-7

26. 26.

    Muller RU, Kubie JL, Saypoff R. The hippocampus as a cognitive graph (abridged version). Hippocampus. 1991;1:243-246.

    Not in our library10.1002/hipo.450010306

27. 27.

    Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. JNeurosci. 1999;19:9497-9507.

    Not in our library10.1523/jneurosci.19-21-09497.1999

28. 28.

    Nitz DA, McNaughton BL. Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. LearnMem. 1999;6:153-167.

    Not in our library

29. 29.

    Nitz D, McNaughton B. Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. JNeurophysiol. 2004;91:863-872.

    Not in our library10.1152/jn.00614.2003

30. 30.

    O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34:171-175.

    Not in our library10.1016/0006-8993(71)90358-1

31. 31.

    O'Keefe J, Nadel L. Hippocampus as a Cognitive Map. 1978.

    Not in our library

32. 32.

    O'Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 1993;3:317-330.

    Not in our library10.1002/hipo.450030307

33. 33.

    O'Neill J, Senior T, Csicsvari J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron. 2006;49:143-155.

    Not in our library10.1016/j.neuron.2005.10.037

34. 34.

    Pepeu G, Giovannini MG. Changes in acetylcholine extracellular levels during cognitive processes. LearnMem. 2004;11:21-27.

    Not in our library10.1101/lm.68104

35. 35.

    Redish AD, Touretzky DS. The role of the hippocampus in solving the Morris water maze. Neural Comput. 1998;10:73-111.

    Not in our library10.1162/089976698300017908

36. 36.

    Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271:1870-1873.

    Not in our library10.1126/science.271.5257.1870

37. 37.

    Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus. 1996;6:149-172.

    Not in our library10.1002/(sici)1098-1063(1996)6:2<149::aid-hipo6>3.0.co;2-k

38. 38.

    Thomson DJ. Spectrum estimation and harmonic analysis. ProcIEEE. 1982;70:1055-1096.

    Not in our library

39. 39.

    Wilson MA, McNaughton BL. Dynamics of the hippocampal ensemble code for space. Science. 1993;261:1055-1058.

    Not in our library10.1126/science.8351520

40. 40.

    Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. JNeurophysiol. 1998;79:1017-1044.

    Not in our library10.1152/jn.1998.79.2.1017

Cited by papers we hold 4

• Neuronal Computation Underlying Inferential Reasoning in Humans and Mice · 2020
  No notice
• The Role of Hippocampal Replay in Memory and Planning · 2018
  No notice
• The content of hippocampal “replay” · 2018
  No notice
• Memory trace replay: the shaping of memory consolidation by neuromodulation · 2015
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.