Theta oscillations and sensorimotor performance.
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Journal: 2005/April - Proceedings of the National Academy of Sciences of the United States of America
ISSN: 0027-8424
Abstract:
Performance and cognitive effort in humans have recently been related to amplitude and multisite coherence of alpha (7-12 Hz) and theta (4-7 Hz) band electroencephalogram oscillations. I examined this phenomenon in rats by using theta band oscillations of the local field potential to signify sniffing as a sensorimotor process. Olfactory bulb (OB) theta oscillations are coherent with those in the dorsal hippocampus (HPC) during odor sniffing in a two-odor olfactory discrimination task. Coherence is restricted to the high-frequency theta band (6-12 Hz) associated with directed sniffing in the OB and type 1 theta in the HPC. Coherence and performance fluctuate on a time scale of several minutes. Coherence magnitude is positively correlated with performance in the two-odor condition but not in extended runs of single odor conditional-stimulus-positive trials. Simultaneous with enhanced OB-HPC theta band coherence during odor sniffing is a significant decrease in lateral entorhinal cortex (EC)-HPC and OB-EC coherence, suggesting that linkage of the olfactory and hippocampal theta rhythms is not through the synaptic relay from OB to HPC in the lateral EC. OB-HPC coupling at the sniffing frequency is proposed as a mechanism underlying olfactory sensorimotor effort as a cognitive process.
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Proc Natl Acad Sci U S A 102(10): 3863-3868
PMID: 15738424

Theta oscillations and sensorimotor performance

Department of Psychology, Institute for Mind and Biology, University of Chicago, 940 East 57th Street, Chicago, IL 60637
E-mail: ude.ogacihcu@yakl.
Edited by Nancy J. Kopell, Boston University, Boston, MA
Edited by Nancy J. Kopell, Boston University, Boston, MA
Received 2004 Oct 25; Accepted 2005 Jan 28.
Copyright © 2005, The National Academy of Sciences

Abstract

Performance and cognitive effort in humans have recently been related to amplitude and multisite coherence of alpha (7-12 Hz) and theta (4-7 Hz) band electroencephalogram oscillations. I examined this phenomenon in rats by using theta band oscillations of the local field potential to signify sniffing as a sensorimotor process. Olfactory bulb (OB) theta oscillations are coherent with those in the dorsal hippocampus (HPC) during odor sniffing in a two-odor olfactory discrimination task. Coherence is restricted to the high-frequency theta band (6-12 Hz) associated with directed sniffing in the OB and type 1 theta in the HPC. Coherence and performance fluctuate on a time scale of several minutes. Coherence magnitude is positively correlated with performance in the two-odor condition but not in extended runs of single odor conditional-stimulus-positive trials. Simultaneous with enhanced OB-HPC theta band coherence during odor sniffing is a significant decrease in lateral entorhinal cortex (EC)-HPC and OB-EC coherence, suggesting that linkage of the olfactory and hippocampal theta rhythms is not through the synaptic relay from OB to HPC in the lateral EC. OB-HPC coupling at the sniffing frequency is proposed as a mechanism underlying olfactory sensorimotor effort as a cognitive process.

Keywords: hippocampus, olfactory bulb, sniffing, behavior, odor discrimination
Abstract

Within a given day, performance measures can change, depending on multiple factors. The neural mechanisms that underlie these performance fluctuations in motor and cognitive tasks remain unexplained, with some studies focusing on theta (4-7 Hz in humans and 4-12 Hz in rats) and alpha (7-12 Hz) oscillations as indicators of cognitive effort associated with performance in difficult tasks (1-6).

The mammalian hippocampus (HPC) and olfactory bulb (OB) are distinguished by high-amplitude theta oscillations of the local field potential. Hippocampal theta rhythm (4-12 Hz in rats) has been shown to accompany locomotion and cognitive processing, and two theta subbands have been described. High-frequency theta (type 1: 6-12 Hz, atropine-resistant) is linked to locomotion, and low-frequency theta (type 2: 4-6 Hz, atropine-sensitive) is seen during immobile states, sensory stimulation, and in urethane-anesthetized animals (7). In the OB, 2- to 12-Hz oscillations have been shown to follow the respiratory cycle with some deviations, and these oscillations are called “theta” principally because they occupy a highly overlapping frequency band with hippocampal theta oscillations (8-13).

HPC theta oscillations and sniffing have been related to performance and learning in previous studies. Theta oscillatory firing of single interneurons in the HPC has been shown to be related to performance in a cognitively demanding olfactory identification task (14). Hippocampal theta oscillations have also been shown to be coherent with sniffing during the initial stages of odor contingency reversal learning (15) and with OB theta oscillations intermittently during exploratory behavior (16).

In this study, I examine the role of theta oscillations in olfactory performance by relating hippocampal theta oscillations recorded from the dorsal HPC at the hilus of the dentate gyrus (DG) to those of similar frequency in the OB during an olfactory identification and response task. The changes in interaction of these two rhythms are tracked within trials and during the course of experimental sessions. A significant positive correlation is shown between OB-HPC theta rhythm coherence (during odor sniffing) and task performance, both of which fluctuate on the order of 5-10 min. This coherence may represent a mechanism whereby sensory, motor, and cognitive structures participate cooperatively in sensory discrimination.

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Acknowledgments

I thank Jennifer Beshel for helpful comments on the manuscript. L.M.K. was supported in part by a Brain Research Foundation Fay/Frank Seed Grant.

Acknowledgments

Notes

Author contributions: L.M.K. designed research, performed research, analyzed data, and wrote the paper.

This paper was submitted directly (Track II) to the PNAS office.

Abbreviations: OB, olfactory bulb; aPC, anterior piriform cortex; EC, entorhinal cortex; DG, dentate gyrus; HPC, hippocampus; CS, conditional stimulus.

Notes
Author contributions: L.M.K. designed research, performed research, analyzed data, and wrote the paper.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations: OB, olfactory bulb; aPC, anterior piriform cortex; EC, entorhinal cortex; DG, dentate gyrus; HPC, hippocampus; CS, conditional stimulus.

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