The Dorsal Hippocampus Neuronal Lesion Does not Affect Theta Activity in the Cortical Network

  • Deepika Kant
  • Sushil K. JhaEmail author
Original Article


The hippocampal theta activity represents the oscillatory field potentials within the range of 4–10 Hz, which mainly appears during wakefulness and rapid eye moment (REM) sleep. The synchronization of theta activity between the hippocampus and other parts of the brain is essential for learning and memory. Theta waves can be recorded from the different cortical areas, which exhibit a consistent phase relationship with hippocampal rhythmicity. It has been postulated that the synchronized theta activity in the cortico-hippocampal networks could be essential for communication of memory information between hippocampus and cortex. It is, however, not known if the dorsal hippocampus (DH) contributes in propagating theta waves in the cortical network. In this study, we have investigated the effects of DH lesion on theta activity during different vigilant states in the frontoparietal cortical network. Rats were surgically prepared for chronic polysomnographic recordings and drug injections. After recovery from surgery, animals were divided into two groups: (a) DH-non-lesioned and (b) DH-lesioned groups. DH was lesioned with microinjection of ibotenic acid. We found that the DH neuronal damage did not significantly alter cortical EEG theta activity. There were only marginal changes in the power of theta (5–9 Hz) and high-frequency oscillatory waves (10–40 Hz) that too only during REM sleep in the DH-lesioned animals. Although the hippocampal theta rhythm plays an important role the cortical–hippocampal synchrony, it is likely that in the absence of DH, the cortical theta oscillation can be modulated by some non-hippocampal theta generators such as the septum-diagonal band of Broca or the supramammillary body.


Dorsal hippocampus Memory REM sleep Theta waves Vigilant states 



This work is supported by DBT, DST (PURSE), UPOE-II, UGC-CAS and UGC-Resource Networking, ICMR funds from India.

Authors Contributions

DK: performed the experiments, generated and analyzed the data, prepared the manuscript. SJ: conceived the idea and designed the work, analyzed the data and finalized the manuscript.

Compliance with Ethical Standards

Conflict of interest

We disclose no conflict of interest. The funding agencies have not played any role in research design, data collection or data analysis.


  1. 1.
    Siapas AG, Lubenov EV, Wilson MA. Prefrontal phase locking to hippocampal theta oscillations. Neuron. 2005;46:141–51.CrossRefGoogle Scholar
  2. 2.
    Winson J. Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr Clin Neurophysiol. 1974;36:291–301.CrossRefGoogle Scholar
  3. 3.
    Kemp IR, Kaada BR. The relation of hippocampal theta activity to arousal, attentive behaviour and somato-motor movements in unrestrained cats. Brain Res. 1975;95:323–42.CrossRefGoogle Scholar
  4. 4.
    Buzsáki G. Theta oscillations in the hippocampus. Neuron. 2002;33:325–40.CrossRefGoogle Scholar
  5. 5.
    Vanderwolf CH. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol. 1969;26:407–18.CrossRefGoogle Scholar
  6. 6.
    Montgomery SM, Sirota A, Buzsaki G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J Neurosci. 2008;28:6731–41.CrossRefGoogle Scholar
  7. 7.
    Tripathi S, Taneja P, Jha SK. Training on an appetitive (Delay)-conditioning task enhances oscillatory waves during sleep in the cortical and Amygdalar Network. Front Behav Neurosci. 2018;12:1–17. Scholar
  8. 8.
    Pavlides C, Greenstein YJ, Grudman M, Winson J. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res. 1988;439:383–7.CrossRefGoogle Scholar
  9. 9.
    Bibbig A, Wennekers T, Palm G. A neural network model of the cortico-hippocampal interplay and the representation of contexts. Behav Brain Res. 1995;66:169–75.CrossRefGoogle Scholar
  10. 10.
    Hutchison IC, Rathore S. The role of REM sleep theta activity in emotional memory. Front Psychol. 2015;6:1439–1439.CrossRefGoogle Scholar
  11. 11.
    Fries P. Rhythms for cognition: communication through coherence. Neuron. 2015;88:220–35.CrossRefGoogle Scholar
  12. 12.
    Lubenov EV, Siapas AG. Hippocampal theta oscillations are travelling waves. Nature. 2009;459:534–9.CrossRefGoogle Scholar
  13. 13.
    Stepan J, Dine J, Fenzl T, Polta SA, von Wolff G, Wotjak CT, et al. Entorhinal theta-frequency input to the dentate gyrus trisynaptically evokes hippocampal CA1 LTP. Front Neural Circuits. 2012;6:1–13. Scholar
  14. 14.
    Patel J, Fujisawa S, Berenyi A, Royer S, Buzsaki G. Traveling theta waves along the entire septotemporal axis of the hippocampus. Neuron. 2012;75:410–7.CrossRefGoogle Scholar
  15. 15.
    Monmaur P, Thomson MA. Hippocampal-dentate theta disturbance after selective CA1 pyramidal cell damage in the rat. Brain Res. 1985;328:301–11.CrossRefGoogle Scholar
  16. 16.
    Leung LS. Generation of theta and gamma rhythms in the hippocampus. Neurosci Biobehav Rev. 1998;22:275–90.CrossRefGoogle Scholar
  17. 17.
    Headley DB, Pare D. Common oscillatory mechanisms across multiple memory systems. NPJ Sci Learn 2017. Google Scholar
  18. 18.
    Robinson J, Manseau F, Ducharme G, Amilhon B, Vigneault E, El Mestikawy S, et al. Optogenetic activation of septal glutamatergic neurons drive hippocampal theta rhythms. J Neurosci. 2016;36:3016–23.CrossRefGoogle Scholar
  19. 19.
    Kumar T, Jha SK. Sleep deprivation impairs consolidation of cued fear memory in rats. PLoS One. 2012;7:e47042.CrossRefGoogle Scholar
  20. 20.
    Tripathi S, Jha SK. Short-term total sleep deprivation alters delay-conditioned memory in the rat. Behav Neurosci. 2016;130:325–35.CrossRefGoogle Scholar
  21. 21.
    Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. The Rat Brain in Stereotaxic Coordinates. Academic Press, Cambridge 2007, pp 1–456.Google Scholar
  22. 22.
    Aton SJ, Seibt J, Dumoulin M, Jha SK, Steinmetz N, Coleman T, et al. Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron. 2009;61:454–66.CrossRefGoogle Scholar
  23. 23.
    Jha SK, Coleman T, Frank MG. Sleep and sleep regulation in the ferret (Mustela putorius furo). Behav Brain Res. 2006;172:106–13.CrossRefGoogle Scholar
  24. 24.
    Kocsis B, Bragin A, Buzsaki G. Interdependence of multiple theta generators in the hippocampus: a partial coherence analysis. J Neurosci. 1999;19:6200–12.CrossRefGoogle Scholar
  25. 25.
    Konopacki J, Bland BH, Roth SH. Carbachol-induced EEG 'theta' in hippocampal formation slices: evidence for a third generator of theta in CA3c area. Brain Res. 1988;451:33–42.CrossRefGoogle Scholar
  26. 26.
    Huerta PT, Lisman JE. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron. 1995;15:1053–63.CrossRefGoogle Scholar
  27. 27.
    Williams JH, Kauer JA. Properties of carbachol-induced oscillatory activity in rat hippocampus. J Neurophysiol. 1997;78:2631–40.CrossRefGoogle Scholar
  28. 28.
    Bland BH, Colom LV. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol. 1993;41:157–208.CrossRefGoogle Scholar
  29. 29.
    Young CK, McNaughton N. Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb Cortex. 2009;19:24–40.CrossRefGoogle Scholar
  30. 30.
    Seidenbecher T, Laxmi TR, Stork O, Pape HC. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science. 2003;301:846–50.CrossRefGoogle Scholar
  31. 31.
    Winson J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science. 1978;201:160–3.CrossRefGoogle Scholar
  32. 32.
    Wetzel W, Ott T, H M. Post-training hippocampal rhythmic slow activity ("theta") elicited by septal stimulation improves memory consolidation in rats. Behav Biol 1977; 21:32-40.CrossRefGoogle Scholar
  33. 33.
    Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsaki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron. 2008;60:683–97.CrossRefGoogle Scholar
  34. 34.
    O'Neill PK, Gordon JA, Sigurdsson T. Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. J Neurosci. 2013;33:14211–24.CrossRefGoogle Scholar
  35. 35.
    Adhikari A, Topiwala MA, Gordon JA. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron. 2010;65:257–69.CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Sleep Research Laboratory, School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia

Personalised recommendations