A Direct Comparison of Theta Power and Frequency to Speed and Acceleration

Kennedy, Jack P; Zhou, Yuchen; Qin, Yu; Lovett, Sarah D.; Sheremet, A.; Burke, Sara N.; Maurer, Andrew P

doi:10.1523/jneurosci.0987-21.2022

Cited by 24 publications

(26 citation statements)

References 47 publications

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“…Moreover, theta contributes to memory consolidation, spatial navigation, nonspatial sequence memory, and working memory (Buzsáki, 2002; Buzsáki and Moser, 2013; Zhang and Jacobs, 2015; Herweg, Solomon and Kahana, 2020; Shahbaba et al ., 2022) - all tasks that require reuniens. However, our understanding of rhythmic prefrontal-reuniens-hippocampal synchrony may be limited due, in part, to the fact that most memory tasks use running behaviors that alone drive theta oscillations irrespective of memory (Hyman et al ., 2005; Allen et al ., 2016; Schultheiss et al ., 2020; Kennedy et al ., 2022).…”

Section: Introductionmentioning

confidence: 99%

Reuniens transiently synchronizes memory networks at beta frequencies

Jayachandran

Viena

Garcia

et al. 2022

Preprint

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Using episodic memories to help guide decisions requires top-down medial prefrontal cortex interactions with the hippocampus. Mechanistically, this integrated prefrontal-hippocampal memory state is thought to be organized by synchronized network oscillations and mediated by connectivity with the nucleus reuniens of the thalamus. Here, we recorded local field potentials from the prefrontal-reuniens-hippocampal network while rats were engaged in a nonspatial sequence memory task which helps isolate memory-related activity from running-related oscillations. We found that synchronous prefrontal-hippocampal beta bursts (15-30 Hz) were dominant during memory trials, whereas synchronous theta (6-12 Hz) was highest during running. Beta rose during a trial and peaked just before a decision, whereas theta was highest during running. Beta bursts first appeared in reuniens and then in prefrontal and hippocampal sites simultaneously, suggesting beta could be directly driven by reuniens. To test this, we used an optogenetic approach (retroAAV-ChR2) to see if reuniens was capable of driving prefrontal-hippocampal beta synchrony. Reuniens activation induced prefrontal-hippocampal beta coherence, and reduced theta coherence, resembling the observed memory-driven network state. These findings demonstrate for the first time that reuniens contributes to memory by driving transient synchronous beta in the prefrontal-hippocampal system facilitating coherent interactions that sub-serve memory-based decision making.

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Section: Introductionmentioning

confidence: 99%

Reuniens transiently synchronizes memory networks at beta frequencies

Jayachandran

Viena

Garcia

et al. 2022

Preprint

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“…Theta oscillations dominate the hippocampus during translational locomotion, with amplitude and frequency positively associated with running speed and acceleration (Kropff et al, 2021;Kennedy et al, 2022). When rats engage in stationary running, (which was not certified by peer review) is the author/funder.…”

Section: Discussionmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted June 22, 2022. ; https://doi.org/10. 1101/2022…”

Section: Discussionmentioning

confidence: 99%

“…Theta oscillations dominate the hippocampus during translational locomotion, with amplitude and frequency positively associated with running speed and acceleration (Kropff et al, 2021; Kennedy et al, 2022). When rats engage in stationary running, however, the absence of linear body movements decouples vestibular and proprioceptive signals, which may dissociate hippocampal theta in two components at 4 and 8 Hz (Safaryan and Mehta, 2021).…”

Section: Discussionmentioning

confidence: 99%

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Hippocampal 4-Hz oscillations emerge during stationary running in a wheel and are resistant to medial septum inactivation

Lima

Belchior

2022

Preprint

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Recent studies described 2-4 Hz oscillations in the hippocampus of rats performing stationary locomotion on treadmills and other apparatus. Since the 2-4 Hz rhythm shares common features with hippocampal theta (5-12 Hz) oscillations - such as a positive running speed-amplitude relationship and modulation of spiking activity - many have questioned whether these rhythms are related or independently generated. To answer this question, we analyzed local field potentials (LFP) and spiking activity from the dorsal CA1 of rats executing a spatial alternation task and running for ~15 s in a wheel during the intertrial intervals both before and after muscimol injection into the medial septum. We observed 4-Hz oscillations during wheel runs, but not during maze runs. The 4-Hz amplitude positively correlated with wheel speed and negatively with maze speed. Also, the amplitude of 4-Hz and theta oscillations were inversely related. Medial septum inactivation abolished hippocampal theta but preserved 4-Hz oscillations. It also affected the entrainment of pyramidal cells and interneurons by 4-Hz rhythmic activity. In all, these results dissociate the underlying mechanism of 4-Hz and theta oscillations in the rat hippocampus.

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“…In humans, it is thought that theta oscillations (4-8 Hz) may support successful spatial exploration and sensorimotor integration during navigation (Burgess & O'Keefe, 2011;Colgin, 2020). For example, speed of travel and path distance have been shown to be related to increased theta power in both animals and humans (Bush et al, 2017;Yassa, 2018;Kennedy et al, 2022). Furthermore, bursts in theta power have been observed during navigational direction-changes (Do et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Theta oscillatory power decreases in humans are associated with spatial learning in a virtual water maze task

Thornberry¹,

Caffrey²,

Commins³

2023

Preprint

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Theta oscillations (4–8 Hz) in humans play a role in navigation processes, including spatial encoding, retrieval, and sensorimotor integration. Increased theta power at frontal and parietal midline regions are known to contribute to successful navigation. However, the dynamics of cortical theta and its role in spatial learning are not fully understood. This study aimed to investigate theta oscillations via EEG during spatial learning in a virtual water maze. Participants were separated into a learning group (n = 25) who learned the location of a hidden goal across twelve trials, or a time-matched non-learning group (n = 25) who were required to simply navigate the same arena, but without a goal. We compared the first trial to the final trial, at two phases of learning, the trial start, and the goal approach. We focused on electrodes at the frontal and parietal midlines. The learning group showed reduced low-frequency theta power at the frontal and parietal midline during the start phase, and largely reduced theta combined with a short but significant increase at both midlines during the goal-approach phase. These patterns were not found in the non-learning group, who instead displayed extensive increases in low-frequency oscillations at both regions during the trial start, and at the parietal midline during goal approach. We suggest our findings provide novel evidence for a link between efficient learning and theta oscillations in humans. Our results also support the theory that theta plays a crucial role in spatial encoding during exploration, as opposed to sensorimotor integration.

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A Direct Comparison of Theta Power and Frequency to Speed and Acceleration

Cited by 24 publications

References 47 publications

Reuniens transiently synchronizes memory networks at beta frequencies

Reuniens transiently synchronizes memory networks at beta frequencies

Hippocampal 4-Hz oscillations emerge during stationary running in a wheel and are resistant to medial septum inactivation

Theta oscillatory power decreases in humans are associated with spatial learning in a virtual water maze task

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