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      Human hippocampal theta power indicates movement onset and distance travelled

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          Abstract

          <p id="d13076259e321">Rodent hippocampal theta-band oscillations are observed throughout translational movement, implicating theta in the encoding of self-motion. Interestingly, increases in theta power are particularly prominent around movement onset. Here, we use intracranial recordings from epilepsy patients navigating in a desktop virtual reality environment to demonstrate that theta power is also increased in the human hippocampus around movement onset and throughout the remainder of movement. Importantly, these increases in theta power are greater both before and during longer paths, directly implicating human hippocampal theta in the encoding of translational movement. These findings help to reconcile previous studies of rodent and human hippocampal theta oscillations and provide additional insight into the mechanisms of spatial navigation in the human brain. </p><p class="first" id="d13076259e324">Theta frequency oscillations in the 6- to 10-Hz range dominate the rodent hippocampal local field potential during translational movement, suggesting that theta encodes self-motion. Increases in theta power have also been identified in the human hippocampus during both real and virtual movement but appear as transient bursts in distinct high- and low-frequency bands, and it is not yet clear how these bursts relate to the sustained oscillation observed in rodents. Here, we examine depth electrode recordings from the temporal lobe of 13 presurgical epilepsy patients performing a self-paced spatial memory task in a virtual environment. In contrast to previous studies, we focus on movement-onset periods that incorporate both initial acceleration and an immediately preceding stationary interval associated with prominent theta oscillations in the rodent hippocampal formation. We demonstrate that movement-onset periods are associated with a significant increase in both low (2–5 Hz)- and high (6–9 Hz)-frequency theta power in the human hippocampus. Similar increases in low- and high-frequency theta power are seen across lateral temporal lobe recording sites and persist throughout the remainder of movement in both regions. In addition, we show that movement-related theta power is greater both before and during longer paths, directly implicating human hippocampal theta in the encoding of translational movement. These findings strengthen the connection between studies of theta-band activity in rodents and humans and offer additional insight into the neural mechanisms of spatial navigation. </p>

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          Most cited references41

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          Place navigation impaired in rats with hippocampal lesions

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            Measuring phase synchrony in brain signals

            This article presents, for the first time, a practical method for the direct quantification of frequency‐specific synchronization (i.e., transient phase‐locking) between two neuroelectric signals. The motivation for its development is to be able to examine the role of neural synchronies as a putative mechanism for long‐range neural integration during cognitive tasks. The method, called phase‐locking statistics (PLS), measures the significance of the phase covariance between two signals with a reasonable time‐resolution (<100 ms). Unlike the more traditional method of spectral coherence, PLS separates the phase and amplitude components and can be directly interpreted in the framework of neural integration. To validate synchrony values against background fluctuations, PLS uses surrogate data and thus makes no a priori assumptions on the nature of the experimental data. We also apply PLS to investigate intracortical recordings from an epileptic patient performing a visual discrimination task. We find large‐scale synchronies in the gamma band (45 Hz), e.g., between hippocampus and frontal gyrus, and local synchronies, within a limbic region, a few cm apart. We argue that whereas long‐scale effects do reflect cognitive processing, short‐scale synchronies are likely to be due to volume conduction. We discuss ways to separate such conduction effects from true signal synchrony. Hum Brain Mapping 8:194–208, 1999. © 1999 Wiley‐Liss, Inc.
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              Intracellular dynamics of hippocampal place cells during virtual navigation

              Hippocampal place cells encode spatial information in rate and temporal codes. To examine the mechanisms underlying hippocampal coding, we measured the intracellular dynamics of place cells by combining in vivo whole cell recordings with a virtual reality system. Head-restrained mice, running on a spherical treadmill, interacted with a computer-generated visual environment to perform spatial behaviors. Robust place cell activity was present during movement along a virtual linear track. From whole cell recordings, we identified three subthreshold signatures of place fields: (1) an asymmetric ramp-like depolarization of the baseline membrane potential; (2) an increase in the amplitude of intracellular theta oscillations; and, (3) a phase precession of the intracellular theta oscillation relative to the extracellularly-recorded theta rhythm. These intracellular dynamics underlie the primary features of place cell rate and temporal codes. The virtual reality system developed here will enable new experimental approaches to study the neural circuits underlying navigation.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                November 14 2017
                November 14 2017
                November 14 2017
                October 24 2017
                : 114
                : 46
                : 12297-12302
                Article
                10.1073/pnas.1708716114
                5699050
                29078334
                f0296cf2-f5c2-4851-a8cf-e676bf659325
                © 2017

                Free to read

                http://www.pnas.org/site/misc/userlicense.xhtml

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