Theta Dynamics in Rat: Speed and Acceleration Across the Septotemporal Axis

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 May 21

PMID 24842406

Citations 16

Authors

Lauren L Long

James R Hinman

Chi-Ming Chen

Monty A Escabi

James J Chrobak

Affiliations

Soon will be listed here.

Abstract

Theta (6-12 Hz) rhythmicity in the local field potential (LFP) reflects a clocking mechanism that brings physically isolated neurons together in time, allowing for the integration and segregation of distributed cell assemblies. Variation in the theta signal has been linked to locomotor speed, sensorimotor integration as well as cognitive processing. Previously, we have characterized the relationship between locomotor speed and theta power and how that relationship varies across the septotemporal (long) axis of the hippocampus (HPC). The current study investigated the relationship between whole body acceleration, deceleration and theta indices at CA1 and dentate gyrus (DG) sites along the septotemporal axis of the HPC in rats. Results indicate that whole body acceleration and deceleration predicts a significant amount of variability in the theta signal beyond variation in locomotor speed. Furthermore, deceleration was more predictive of variation in theta amplitude as compared to acceleration as rats traversed a linear track. Such findings highlight key variables that systematically predict the variability in the theta signal across the long axis of the HPC. A better understanding of the relative contribution of these quantifiable variables and their variation as a function of experience and environmental conditions should facilitate our understanding of the relationship between theta and sensorimotor/cognitive functions.

Citing Articles

Spatial Coding Dysfunction and Network Instability in the Aging Medial Entorhinal Cortex.

Herber C, Pratt K, Shea J, Villeda S, Giocomo L bioRxiv. 2024; .

PMID: 38659809 PMC: 11042240. DOI: 10.1101/2024.04.12.588890.

Repeated Binge Alcohol Drinking Leads to Reductions in Corticostriatal Theta Coherence in Female but not Male Mice.

Ardinger C, Lapish C, Linsenbardt D bioRxiv. 2024; .

PMID: 38496601 PMC: 10942409. DOI: 10.1101/2024.03.07.581791.

Automated system for training and assessing reaching and grasping behaviors in rodents.

Jordan G, Vishwanath A, Holguin G, Bartlett M, Tapia A, Winter G J Neurosci Methods. 2023; 401:109990.

PMID: 37866457 PMC: 10731814. DOI: 10.1016/j.jneumeth.2023.109990.

Phase relations of interneuronal activity relative to theta rhythm.

Mysin I Front Neural Circuits. 2023; 17:1198573.

PMID: 37484208 PMC: 10358363. DOI: 10.3389/fncir.2023.1198573.

Theta/gamma Co-modulation Disruption After NMDAr Blockade by MK-801 Is Associated with Spatial Working Memory Deficits in Mice.

Abad-Perez P, Molina-Paya F, Martinez-Otero L, Borrell V, Redondo R, Brotons-Mas J Neuroscience. 2023; 519:162-176.

PMID: 36990270 PMC: 10229075. DOI: 10.1016/j.neuroscience.2023.03.022.

References

Law J, Flanery M, Wirth S, Yanike M, Smith A, Frank L . Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. J Neurosci. 2005; 25(24):5720-9. PMC: 6724878. DOI: 10.1523/JNEUROSCI.4935-04.2005. View

MCFARLAND W, TEITELBAUM H, Hedges E . Relationship between hippocampal theta activity and running speed in the rat. J Comp Physiol Psychol. 1975; 88(1):324-8. DOI: 10.1037/h0076177. View

Bouwman B, van Lier H, Nitert H, Drinkenburg W, Coenen A, van Rijn C . The relationship between hippocampal EEG theta activity and locomotor behaviour in freely moving rats: effects of vigabatrin. Brain Res Bull. 2005; 64(6):505-9. DOI: 10.1016/j.brainresbull.2004.10.006. View

Marrelec G, Horwitz B, Kim J, Pelegrini-Issac M, Benali H, Doyon J . Using partial correlation to enhance structural equation modeling of functional MRI data. Magn Reson Imaging. 2007; 25(8):1181-9. DOI: 10.1016/j.mri.2007.02.012. View

Salvador R, Suckling J, Coleman M, Pickard J, Menon D, Bullmore E . Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex. 2005; 15(9):1332-42. DOI: 10.1093/cercor/bhi016. View

Lorch Jr R, Myers J . Regression analyses of repeated measures data in cognitive research. J Exp Psychol Learn Mem Cogn. 1990; 16(1):149-57. DOI: 10.1037//0278-7393.16.1.149. View

Gray C . Synchronous oscillations in neuronal systems: mechanisms and functions. J Comput Neurosci. 1994; 1(1-2):11-38. DOI: 10.1007/BF00962716. View

Montgomery S, Betancur M, Buzsaki G . Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J Neurosci. 2009; 29(5):1381-94. PMC: 2768079. DOI: 10.1523/JNEUROSCI.4339-08.2009. View

Berry S, Rinaldi P, Thompson R, Verzeano M . Analysis of temporal relations among units and slow waves in rabbit hippocampus. Brain Res Bull. 1978; 3(5):509-18. DOI: 10.1016/0361-9230(78)90080-1. View

10.

Hinman J, Penley S, Long L, Escabi M, Chrobak J . Septotemporal variation in dynamics of theta: speed and habituation. J Neurophysiol. 2011; 105(6):2675-86. DOI: 10.1152/jn.00837.2010. View

11.

Jones M, Wilson M . Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 2005; 3(12):e402. PMC: 1283536. DOI: 10.1371/journal.pbio.0030402. View

12.

Nyhus E, Curran T . Functional role of gamma and theta oscillations in episodic memory. Neurosci Biobehav Rev. 2010; 34(7):1023-35. PMC: 2856712. DOI: 10.1016/j.neubiorev.2009.12.014. View

13.

Lee M, Chrobak J, Sik A, Wiley R, Buzsaki G . Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience. 1994; 62(4):1033-47. DOI: 10.1016/0306-4522(94)90341-7. View

14.

Smith P, Horii A, Russell N, Bilkey D, Zheng Y, Liu P . The effects of vestibular lesions on hippocampal function in rats. Prog Neurobiol. 2005; 75(6):391-405. DOI: 10.1016/j.pneurobio.2005.04.004. View

15.

Buzsaki G, Chrobak J . Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol. 1995; 5(4):504-10. DOI: 10.1016/0959-4388(95)80012-3. View

16.

Bland B, Oddie S . Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav Brain Res. 2001; 127(1-2):119-36. DOI: 10.1016/s0166-4328(01)00358-8. View

17.

Harris K, Csicsvari J, Hirase H, Dragoi G, Buzsaki G . Organization of cell assemblies in the hippocampus. Nature. 2003; 424(6948):552-6. DOI: 10.1038/nature01834. View

18.

Ulanovsky N, Moss C . Hippocampal cellular and network activity in freely moving echolocating bats. Nat Neurosci. 2007; 10(2):224-33. DOI: 10.1038/nn1829. View

19.

Lisman J . The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus. 2005; 15(7):913-22. DOI: 10.1002/hipo.20121. View

20.

Jutras M, Fries P, Buffalo E . Gamma-band synchronization in the macaque hippocampus and memory formation. J Neurosci. 2009; 29(40):12521-31. PMC: 2785486. DOI: 10.1523/JNEUROSCI.0640-09.2009. View