Theta Oscillations and Comparator Function of the Hippocampus

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Responses triggered by change/novelty of the stimuli are fundamental to adaptive behavior. By comparing the current observation with the previous one, living organisms can make predictions and change their actions. Brain mechanisms and its structures involved in the comparator function have not yet been fully elucidated. The evidence accumulated emphasizes the particular importance of the hippocampus in the comparator system; it is shown that novelty detection is carried out by hippocampal neurons through the implementation of the match-mismatch mechanism or divergence. This paper includes information on existing hypotheses that propose how these mechanisms are implemented, what other brain structures are involved in mismatch detection, how they are connected to the hippocampus, and what processes contribute to this function. It is assumed, in particular, that it is not novelty per se, but rather that one that contrasts with previously acquired experience and initiates the process of divergence. The arguments are analyzed that the theta rhythm plays a key role in the functioning of the hippocampus as a comparator. Theta oscillations caused by the appearance of a new signal/change in the environment, mediate, in particular, the mechanism of temporal coordination of structures involved in the comparator function. In the comparator system, the theta rhythm acts as a filter: it participates in the selection and transmission of a new signal to registration of information in the hippocampus. Increases in theta oscillations and their coherence in brain structures that process new information serve as a signal of mismatch, facilitating a change in behavioral strategy. Gamma-oscillations, like the theta rhythm, also play a significant role in the comparator system: during generation of the theta rhythm in the prefrontal cortex, temporal coincidence of gamma-oscillations in other brain regions with certain phase of the thetha cycle may serve as the comparator function in the process of memorization. A deeper understanding of the mechanisms of the comparator function or mechanisms of its damage will give us a better idea about the treatment of disorders, such as schizophrenia, Alzheimer’s disease, temporal lobe epilepsy and many others.

About the authors

V. F Kitchigina

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

Email: vkitchigina@gmail.com
Pushchino, Russia

References

  1. Mumford D. On the computational architecture of the neocortex. I. The role of the thalamo-cortical loop. Biol. Cybern., 65, 135 (1991). doi: 10.1007/BF00202389
  2. Mumford D. On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biol. Cybern., 66, 241 (1992). doi: 10.1007/BF00198477
  3. Friston K. A theory of cortical responses. Philos. Trans. Roy. Soc. Lond. B. Biol. Sci., 360, 815–836 (2005). doi: 10.1098/rstb.2005.1622
  4. Garrido M. I., Sahani M., and Dolan R. J. Outlier Responses Reflect Sensitivity to Statistical Structure in the Human Brain. PLoS Comput. Biol., 9 (3), e1002999 (2013). doi: 10.1371/journal.pcbi.1002999
  5. Garrido M. I., Barnes G. R., Kumaran D., Maguire E. A., and Dolan R. J. Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations. NeuroImage, 120, 362–370 (2015). doi: 10.1016/j.neuroimage.2015.07.016
  6. Numan R. A prefrontal-hippocampal comparator for goal-directed behavior: the intentional self and episodic memory. Front Behav Neurosci., 9, 323 (2015). doi: 10.3389/fnbeh.2015.00323
  7. Vinogradova O. S. Expression, control, and probable functional significance of the neuronal theta-rhythm. Progr. Neurobiol., 45 (6), 523 (1995). doi: 10.1016/0301-0082(94)00051-i
  8. Numan R. Cortical-limbic mechanisms and response control: a theoretical review. Physiol. Psychol., 6, 445 (1978). doi: 10.3389/fnbeh.2015.00323
  9. Numan R. Septal modulation of the working memory for voluntary behavior. In: The behavioral neuroscience of the septal region. Ed. by R. Numan (Springer-Verlag, NewYork, 2000), pp. 298–326.
  10. Duncan K., Ketz N., Inati S. J., and Davachi L. Evidence for area CA1 as a match/mismatch detector: a high-resolution fMRI study of the human hippocampus. Hippocampus, 22, 389–398 (2012). doi: 10.1002/hipo.20933
  11. Von Holst E. Relations between the central nervous system and the peripheral organs. Br. J. Anim. Behav., 2 (3), 289–294 (1954). doi: 10.1016/S0950-5601(54)80044-X
  12. Miller G. A., Galanter E. and Pribram K. H. Plans and the structure of behavior, Ed. by H. Rinehart & Winston (New York, 1960).
  13. Anokhin P. K. Cybernetic sand the integrative activity of the brain. In: A handbook of contemporary soviet psychology, Ed. by M. Coleand and I. Maltzman (BasicBooks, New York, 1969), pp. 830–856.
  14. Vinogradova O. S. Registration of information and the limbic system. In: Short-term changes in neural activity and behavior, Ed. by G. Horn and R. A. Hinde (Cambridge University Press, Cambridge, 1970), pp. 95–140.
  15. Виноградова О. С. Гиппокамп и память (Наука, М., 1975).
  16. Виноградова О. С., Бражник Е. С., Кичигина В. Ф. и Стафехина В. С. Роль афферентных входов в организации нейронной активности гиппокампа как компаратора. In: Gagra Symp. Proc., vol. 7 (Mezniereba Publ. House, Tbilisi, 1981), pp. 288–307.
  17. Vinogradova O. S., Brazhnik E. S., Kitchigina V. F. and Stafekhina V. S. Acetylcholine, theta-rhythm and activity of the hippocampal neurons in the rabbit. IV. Sensory stimulation. Neuroscience, 53 (4), 993-1007 (1993). doi: 10.1016/0306-4522(93)90484-w
  18. Vinogradova O. S. Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog. Neurobiol., 45 (6), 523–583 (1995). doi: 10.1016/0301-0082(94)00051-i.
  19. Vinogradova O. S. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus, 11, 578–598 (2001). doi: 10.1002/hipo.1073
  20. Numan R. The effects of frontal and septal ablation on response regulation in the cat (Doctoral dissertation, University of Tennessee, 1972). Dissertation Abstr. Int., 33 (11), 5545B–5546B (1973).
  21. Numan R. Cortical-limbic mechanisms and response control: a theoretical review. Physiol. Psychol., 6, 445–470 (1978). doi: 10.3758/BF03326750
  22. Numan R. Septal modulation of the working memory for voluntary behavior. In: The Behavioral Neuroscience of the Septal Region, Ed. by R. Numan (Springer-Verlag, New York, 2000), pp. 298–326.
  23. Numan R. The prefrontal-hippocampal comparator: volition and episodic memory. Percept. Mot. Skills, 128 (6), 2421–2447 (2021). doi: 10.1177/00315125211041341
  24. Gray J. A. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system (Oxford University Press, New York, 1982).
  25. Griffiths K. R., Morris R. W., and Balleine B. W. Translational studies of goal-directed action as a framework for classifying deficits across psychiatric disorders. Front. Syst. Neurosci., 8, 101 (2014). doi: 10.3389/fnsys.2014.00101
  26. Eichenbaum H., Fagan A., Mathews P., and Cohen N. J. Hippocampal system dysfunction and odor discrimination learning in rats: impairmentor facilitation depending on representational demands. Behav. Neurosci., 102, 331–339 (1988). doi: 10.1037/0735-7044.102.3.331
  27. Ennaceur A. and Meliani K. A new one-trial test for neurobiological studies of memoryinrats. III. Spatial vs. non-spatial working memory. Behav. Brain Res., 51, 83–92 (1992). doi: 10.1016/s0166-4328(05)80315-8
  28. Kelsey J. E. and Vargas H. Medial septal lesions disrupt spatial, but not nonspatial, working memory in rats. Behav. Neurosci., 107 (5), 65–574 (1993). doi: 10.1037//0735-7044.107.4.565
  29. Cho Y. H. and Kesner R. P. Relational object association learning in rats with hippocampal lesions. Behav. Brain Res. 67, 91–98 (1995). doi: 10.1016/0166-4328(94)00109-s
  30. Gaffan E. A., Bannerman D. M., Warburton E. C. and Aggleton J. P. Rats processing of visual scenes: effects of lesions to fornix, anterior thalamus, mammillary nuclei or the retrohippocampal region. Behav. Brain Res., 121, 103–11 (2001). doi: 10.1016/0166-4328(94)00109-s
  31. Janisewicz A. M., and Baxter M. G. Transfer effects and conditional learning in rats with selective lesions of medial septal/diagonal band cholinergic neurons. Behav. Neurosci., 117, 1342–1352 (2003). doi: 10.1037/0735-7044.117.6.1342
  32. M’Harzi M. and Jarrard L. Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task. Behav. Brain Res., 49, 159–165 (1992). doi: 10.1016/S0166-4328(05)80160-3
  33. Fyhn M., Molden S., Hollup S., Moser M. B. and Moser E. I. Hippocampal neurons responding to firsttime dislocation of a target object. Neuron, 35, 555–566 (2002). doi: 10.1016/s0896-6273(02)00784-5
  34. Kumaran D. and Maguire E. A. An unexpected sequence of events: Mismatch detection in the human hippocampus. PLoS Biol., 4 (12), e424 (2006). doi: 10.1371/journal.pbio.0040424
  35. Chen J., Olsen R. K., Preston A. R., Glover G. H., and Wagner A. D. Associative retrieval processes in the human medial temporal lobe: hippocampal retrieval success and CA1 mismatch detection. Learn. Mem., 18, 523–528 (2011). doi: 10.1101/lm.2135211
  36. Berteau S. and Bullock D. J. Simulations reveal how M-currents and memory-based inputs from CA3 enable single neuron mismatch detection for EC3 inputs to the CA1 subfield of hippocampus. J. Neurophysiol., 124, 544–556 (2020). doi: 10.1152/jn.00238.2019
  37. Lisman J. E. and Grace A. A. The hippocampal-VTA loop: controlling the entry of information in to longterm memory. Neuron, 46, 703–713 (2005). doi: 10.1016/j.neuron.2005.05.002
  38. Santos-Pata D., Amil A. F., Raikov I. G., RennoCosta C., Mura A., Soltesz I., Verschure P. F. M. J. Entorhinal mismatch: a model of self-supervised learning in the hippocampus. iScience, 24 (4), 102364 (2021). doi: 10.1016/j.isci.2021.102364
  39. Sik A., Ylinen A., Penttonen M. and Buzsaki G. Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science, 265, 1722–1724, (1994). doi: 10.1126/science.8085161
  40. Melzer S., Michael M., Caputi A., Eliava M., Fuchs E. C., Whittington M. A., and Monyer H. Longrangeprojecting gabaergic neurons modulate inhibition in hippocampus and entorhinal cortex. Science, 335, 1506–1510, (2012). doi: 10.1126/science.1217139
  41. Lőrincz A. and Buzsaki G. Two-phase computational model training long-term memories in the entorhinalhippocampal region. Ann. N. Y. Acad. Sci., 911, 83 (2000). doi: 10.1111/j.1749-6632.2000.tb06721.x
  42. Bland B. H. T. The medial septum: Node of the ascending brainstem hippocampal synchronizing pathways. In: The behavioral neuroscience of the septal region, Ed. by R. Numan (Springer-Verlag, 2000), pp. 115–145.
  43. Buzsaki G. Theta oscillations in the hippocampus. Neuron, 33, 325–340 (2002). doi: 10.1016/s0896-6273(02)00586-x
  44. Lewis P. R. and Shute C. C. D. The cholinergicl imbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain, 90, 521–540 (1967). doi: 10.1093/brain/90.3.521
  45. Amaral D. G. and Kurz J. An analysis of the origins of the cholinergic and non cholinergic septal projections to the hippocampal formation of the rat. J. Comp. Neurol., 240, 37–59 (1985). doi: 10.1002/cne.902400104
  46. Mysin I. A Model of the CA1 field rhythms. ENEURO, 8 (6), 0192-21.2021 (2021).
  47. Green J. D. and Arduini A. A. Hippocampal electrical activity in arousal. J. Neurophysiol., 17, 533–557 (1954). doi: 10.1523/ENEURO.0192-21.2021
  48. Donovick P. J. Effects of localized septal lesions on hippocampal EEG activity and behavior in rats. J. Comp. Physiol. Psychol., 66, 569–578 (1968). doi: 10.1037/h0026514
  49. Бражник Е. С. и Виноградова О. С. Нейронная активность «изолированного гиппокампа». Журн. высш. нерв. деят. им. И.П. Павлова, 28, 372 (1978).
  50. Виноградова О. С., Бражник Е. С., Кичигина В. Ф. и Стафехина В. С. Тета-модуляция гиппокампальных нейронов у кролика и ее корреляция с другими параметрами спонтанной и вызванной активности. Журн. высш. нерв. деятельности им. И.П. Павлова, 42, 95-111 (1992).
  51. Кичигина В. Ф., Кудина Т. А., Зенченко К. И. и Виноградова О. С. Фоновая активность нейронов гиппокампа кролика при функциональном отключении структур, регулирующих тета-ритм. Журн. высш. нерв. деятельности им. И.П. Павлова, 48, 505-515 (1998).
  52. Кичигина В. Ф. Механизмы регуляции и функциональное значение тета-осцилляций в септо-гиппокампальной системе мозга. Диc. … д-pа биол. наук (ИТЭБ РАН, Пущино, 2006).
  53. Olton D. S., Walker J. A. and Wolf W. A. A disconnection analysis of hippocampal function. Brain Res., 233, 241–253 (1982). doi: 10.1016/0006-8993(82)91200-8
  54. Walsh T. J. The medial septum and working/episodic memory. In The behavioral neuroscience of the septal region, Ed. by R. Numan (Springer-Verlag, New York, 2000), pp. 327–362.
  55. Pang K. C., Jiao X., Sinha S., Beck K. D. and Servatius R. J. Damage of GABA extinction of active avoidance: effects on proactive interference. Hippocampus, 21, 835–846 (2011). doi: 10.1002/hipo.20799
  56. Vanderwolf C. H. Limbic-diencephalic mechanisms of voluntary movement. Psychol. Rev., 78 (8), 3–113 (1971). doi: 10.1037/h0030672
  57. Buzsaki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus, 15, 827–840 (2005). doi: 10.1002/hipo.20113
  58. Petsche H., Gogolak G., and Zwieten P. A. Rhythmicity of septal cell discharges at various levels of reticular excitation. EEG. Clin. Neurophysiol. 19, 25–33 (1965). doi: 10.1016/0013-4694(65)90004-0
  59. Бражник Е. С. и Виноградова О. С. Влияние полной подрезки септум на активность ее нейронов. Журн. высш. нерв. деят. им. И.П. Павлова, 30, 141–152 (1980).
  60. Бражник Е. С. Сравнительные характеристики залповых нейронов септум при устранении восходящих влияний ретикулярной формации у кроликов (хирургическими и фармакологическими воздействиями). Журн. высш. нерв. деятельности им. И.П. Павлова, 36, 721–729 (1986).
  61. Stewart M. and Fox S. E. Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci., 13 (5), 163–168 (1990). doi: 10.1016/0166-2236(90)90040-h
  62. Kitchigina V. F., Vinogradova O. S., and Bragin A. G. Neuronal activity of the septum transplanted into the neocortical barrel field of the rat. Restorative Neurology & Neurosci., 2, 109–122 (1991). doi: 10.3233/RNN-1991-2301
  63. Sweeney J. E., Lamour Y., and Bassant M. H. Arousaldependent properties of medial septal neurons in the ananesthetized rat. Neuroscience, 48, 353–362 (1992). doi: 10.1016/0306-4522(92)90495-n
  64. Brazhnik E. S. and Fox S. E. Intracellular recordings from medial septal neurons during hippocampal theta rhythm. Exp. Brain Res., 114, 442–453 (1997). doi: 10.1007/pl00005653
  65. Vinogradova O. S., Kitchigina V. F., and Zenchenko C. I. Pacemaker neurons of the forebrain medial septal area and theta rhythm of the hippocampus. Membr. Cell. Biol., 11, 715–725 (1998). PMID: 9718568
  66. Segal M. and Bloom F. E. The action of norepinephrine in the rat hippocampus. III. Hippocampal cellular responses to locus coeruleus stimulation in the awake rat. Brain Res., 107 (3), 499–511 (1976). doi: 10.1016/0006-8993(76)90140-2
  67. Yamomoto T., Watanabe S., Oishi R., and Ueki S. Effects of midbrain raphe stimulation and lesion on EEG activity in rats. Brain Res. Bull., 4, 491–495 (1977). doi: 10.1016/0361-9230(79)90033-9
  68. Бражник Е. С., Виноградова О. С., Стафехина В. С. и Кичигина В. Ф. Спонтанная активность гиппокампальных нейронов во время модуляции тетаритма холинергическими веществами. Журн. высш. нерв. деятельности им. И.П. Павлова, 42 (5), 944–954 (1992).
  69. Кичигина В. Ф. и Гордеева Т. А. Регуляция септального пейсмекера тета-ритма ядрами шва среднего мозга. Журн. высш. нерв. деятельности им. И.П. Павлова, 45, 848–859 (1995).
  70. Vertes R. P. and Kocsis B. Brainstem-diencephalo-septohippocampal system controlling the theta rhythm of the hippocampus. Neuroscience, 81 (4), 893–926 (1997). doi: 10.1016/s0306-4522(97)00239-x
  71. Vinogradova O. S., Kitchigina V. F., Kudina T. A., and Zhenchenko K. I. Spontaneous activity and sensory responses of hippocampal neurons during persistent theta rhythm evoked by median raphe nucleus blockade in rabbit. Neuroscience, 94, 745–753 (1999). doi: 10.1016/s0306-4522(99)00253-5
  72. Кичигина В. Ф. и Кутырева Е. В. Модуляция тетаактивности в септо-гиппокампальной системе агонистов альфа2-адренорецепторов клонидином. Журн. высш. нерв. деятельности им. И.П. Павлова, 52, 195–204 (2002).
  73. Kitchigina V. F., Kutyreva E. V. and Brazhnik E. S. Modulation of theta rhythmicity in the medial septal neurons and hippocampal EEG in the awake rabbit via actions at noradrenergic α2-receptors. Neuroscience, 120, 509–521 (2003). doi: 10.1016/s0306-4522(03)00331-2
  74. Anderson K. L., Rajagovindan R., Ghacibeh G. A., Meador K. J., and Ding M. Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb. Cortex, 20, 1604–1612 (2010). doi: 10.1093/cercor/bhp223
  75. Fell J. and Axmacher N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci., 12, 105–118 (2011). doi: 10.1038/nrn2979
  76. Sauseng P., Griesmayr B., Freunberger R. and Klimesch W. Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci. Biobehav. Rev. 34, 1015–1022 (2010). doi: 10.1016/j.neubiorev.2009.12.006
  77. Kaplan R., Doeller C.F., Barnes G.R., Litvak V., Duzel E., Bandettini P.A. and Burgess N. Movementrelated theta rhythm in humans: coordinating self-directed hippocampal learning. PLoS. Biol., 10, e1001267 (2012). doi: 10.1371/journal.pbio.1001267
  78. Penley S. C., Hinman J. R., Long L. L., Markus E. J., Escabi M. A., and Chrobak J. J. Novel space alters theta and gamma synchrony across the longitudinal axis of the hippocampus. Front. Syst. Neurosci., 7, 20. (2013). doi: 10.3389/fnsys.2013.00020
  79. Yang S., Yang S., Moreira T., Hoffman G., Carlson G. C., Bender K. J., Bradley A. E., and Tang C.-M. Interlamellar CA1 network in the hippocampus. Proc. Natl. Acad. Sci. USA, 111, 12919–12924 (2014). doi: 10.1073/pnas.1405468111
  80. Long L. L., Bunce J. G., and Chrobak J. J. Theta variation and spatiotemporal scaling along the septotemporal axis of the hippocampus. Front. Syst. Neurosci., 9, 37 (2015). doi: 10.3389/fnsys.2015.00037
  81. Benchenane K., Peyrache A., Khamassi M., Tierney P. L., Gioanni Y., Battaglia F. P., and Wiener S. I. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron, 66, 921–936 (2010). doi: 10.1016/j.neuron.2010.05.013
  82. Zou D., Aitake M., Hori E., Umeno K., Fukuda M., Ono T., and Nishijo H. Rat hippocampal theta rhythm during sensory mismatch. Hippocampus, 19, 350–359 (2009). doi: 10.1002/hipo.20524
  83. Aitake M., Hori E., Matsumoto J., Umeno K., Fukuda M., Ono T., and Nishijo H. Sensory mismatch induces autonomic responses associated with hippocampal theta waves in rats. Behav. Brain Res., 220, 244–253 (2011). doi: 10.1016/j.bbr.2011.02.011
  84. Cavanagh J. F., Cohen M. X., and Allen J. J. Prelude to and resolution of anerror: EEG phase synchrony reveals cognitive control dynamics during action monitoring. J. Neurosci., 29, 98–105 (2009). doi: 10.1523/JNEUROSCI.4137-08.2009
  85. Del Arco A., Park J., Wood J., Kim Y., and Moghaddam B. Adaptive encoding of outcome prediction by prefrontal cortex ensembles supports behavioral flexibility. J. Neurosci., 37 (35), 8363–8373 (2017). doi: 10.1523/JNEUROSCI.0450-17.2017
  86. Schultz W. Getting formal with dopamine and reward. Neuron, 36, 241–263 (2002).
  87. Holroyd C. B. and Coles M. G. The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol. Rev., 109, 67–709 (2002). doi: 10.1037/0033-295X.109.4.679
  88. Olvera-Cortes E., Cervantes M., and Gonzalez-Burgos I. , Place-learning, but not cue-learning training, modifies the hippocampal theta rhythm in rats. Brain Res. Bull., 58, 261 (2002). doi: 10.1016/s0361-9230(02)00769-4
  89. Sakimoto Y., Hattori M., Takeda K., Okada K., Sakata S. Hippocampal theta wave activity during configural and non-configural tasks in rats. Exp. Brain Res.,225, 177–185 (2013). doi: 10.1007/s00221-0123359-2

Copyright (c) 2024 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies