Theta Oscillations in the Human Medial Temporal Lobe during Real World Ambulatory Movement

AbstractTheta oscillations play a critical role in learning and memory by coordinating the spiking activity of neuronal ensembles via mechanisms such as spike timing dependent plasticity1–7. This rhythm is present in rodents where it is continuously evident during movement at frequencies within 6-12Hz8,9. In humans, however, the presence of continuous theta rhythm has been elusive; indeed, a functionally similar theta is thought to occur at lower frequency ranges (3-7Hz) and in shorter bouts10–12. This lower frequency theta rhythm is observed during a variety of behaviors, including virtual navigation, but has never been tested during real world ambulatory movement. Here we examined the oscillatory properties of theta within the human medial temporal lobe (MTL) in freely moving human subjects chronically implanted with the clinical NeuroPace RNS® responsive neurostimulator device, capable of wireless recordings of continuous intracranial deep brain electroencephalographic (iEEG) activity. MTL iEEG recordings, together with sub-millimeter position tracking, revealed the presence of high frequency theta oscillations (6-12Hz) during ambulation. The prevalence of these oscillations was increased during fast movement compared to slow movement. These theta bouts, although occurring more frequently, were not significantly different in durations during fast versus slow movements. In a rare opportunity to study one subject with congenital blindness, we found that both the prevalence and duration of theta bouts were much greater than those in sighted subjects. Our results suggest that higher frequency theta indeed exists in humans during movement providing critical support for conserved neurobiological mechanisms for spatial navigation. The precise link between this pattern and its behavioral correlates will be an exciting area for future studies given this novel methodology for simultaneous motion capture and long term chronic recordings from deep brain targets during ambulatory human behavior.

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Theta Oscillations in the Human Medial Temporal Lobe during Real-World Ambulatory Movement

Current Biology ◽

10.1016/j.cub.2017.10.062 ◽

2017 ◽

Vol 27 (24) ◽

pp. 3743-3751.e3 ◽

Cited By ~ 57

Author(s):

Zahra M. Aghajan ◽

Peter Schuette ◽

Tony A. Fields ◽

Michelle E. Tran ◽

Sameed M. Siddiqui ◽

...

Keyword(s):

Temporal Lobe ◽

Real World ◽

Medial Temporal Lobe ◽

Theta Oscillations

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Thalamic-Medial Temporal Lobe Connectivity Underpins Familiarity Memory

Cerebral Cortex ◽

10.1093/cercor/bhz345 ◽

2020 ◽

Vol 30 (6) ◽

pp. 3827-3837 ◽

Cited By ~ 3

Author(s):

Alex Kafkas ◽

Andrew R Mayes ◽

Daniela Montaldi

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Critical Role ◽

Dynamic Interaction ◽

Thalamic Nuclei ◽

Neural Basis ◽

General Role ◽

Anterior Thalamus ◽

Ventrolateral Thalamus ◽

Familiarity And Recollection

Abstract The neural basis of memory is highly distributed, but the thalamus is known to play a particularly critical role. However, exactly how the different thalamic nuclei contribute to different kinds of memory is unclear. Moreover, whether thalamic connectivity with the medial temporal lobe (MTL), arguably the most fundamental memory structure, is critical for memory remains unknown. We explore these questions using an fMRI recognition memory paradigm that taps familiarity and recollection (i.e., the two types of memory that support recognition) for objects, faces, and scenes. We show that the mediodorsal thalamus (MDt) plays a material-general role in familiarity, while the anterior thalamus plays a material-general role in recollection. Material-specific regions were found for scene familiarity (ventral posteromedial and pulvinar thalamic nuclei) and face familiarity (left ventrolateral thalamus). Critically, increased functional connectivity between the MDt and the parahippocampal (PHC) and perirhinal cortices (PRC) of the MTL underpinned increases in reported familiarity confidence. These findings suggest that familiarity signals are generated through the dynamic interaction of functionally connected MTL-thalamic structures.

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The Medial Temporal Lobe Is Critical for Spatial Relational Perception

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01583 ◽

2020 ◽

Vol 32 (9) ◽

pp. 1780-1795 ◽

Cited By ~ 1

Author(s):

Nicholas A. Ruiz ◽

Michael R. Meager ◽

Sachin Agarwal ◽

Mariam Aly

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Critical Role ◽

Long Term Memory ◽

Term Memory ◽

Cognitive Domains ◽

Attention Tasks ◽

Human Participants ◽

Attention And Perception

The medial temporal lobe (MTL) is traditionally considered to be a system that is specialized for long-term memory. Recent work has challenged this notion by demonstrating that this region can contribute to many domains of cognition beyond long-term memory, including perception and attention. One potential reason why the MTL (and hippocampus specifically) contributes broadly to cognition is that it contains relational representations—representations of multidimensional features of experience and their unique relationship to one another—that are useful in many different cognitive domains. Here, we explore the hypothesis that the hippocampus/MTL plays a critical role in attention and perception via relational representations. We compared human participants with MTL damage to healthy age- and education-matched individuals on attention tasks that varied in relational processing demands. On each trial, participants viewed two images (rooms with paintings). On “similar room” trials, they judged whether the rooms had the same spatial layout from a different perspective. On “similar art” trials, they judged whether the paintings could have been painted by the same artist. On “identical” trials, participants simply had to detect identical paintings or rooms. MTL lesion patients were significantly and selectively impaired on the similar room task. This work provides further evidence that the hippocampus/MTL plays a ubiquitous role in cognition by virtue of its relational and spatial representations and highlights its important contributions to rapid perceptual processes that benefit from attention.

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Spatial mnemonic encoding: Theta power decreases co-occur with medial temporal lobe BOLD increases during the usage of the Method of Loci

10.1101/052720 ◽

2016 ◽

Cited By ~ 1

Author(s):

M.-C. Fellner ◽

G. Volberg ◽

M. Wimber ◽

M. Goldhacker ◽

M. W. Greenlee ◽

...

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Negative Relationship ◽

Low Frequency ◽

Theta Oscillations ◽

Oscillatory Activity ◽

Bold Signal ◽

Memory Processes ◽

Theta Power ◽

Method Of Loci

AbstractThe Method of Loci is one, if not the most, efficient mnemonic encoding strategy. This strategy combines the core cognitive processes commonly linked to medial temporal lobe (MTL) activity: spatial processing and associative memory processes. During such tasks fMRI studies consistently demonstrate increases in medial temporal lobe (MTL) activity, while electrophysiological studies have emphasized the important role of theta oscillations (3-8 Hz) in the MTL. How MTL activity is linked to theta oscillatory EEG power, however, is unknown. Specifically, it is not known whether increases or decreases in MTL theta power are associated with increased BOLD signal. To investigate this question we recorded EEG and fMRI while participants used the spatial Method of Loci contrasted to the Pegword Method, a similarly associative but non spatial mnemonic. Surprisingly, the more effective spatial mnemonic induced a pronounced theta power decrease in the left MTL compared to the non-spatial associative mnemonic strategy. This effect was mirrored by BOLD signal increases in the MTL. This pattern of results suggests that theta oscillations in the MTL are negatively related to BOLD signal increases. These findings extend the well-known negative relation of alpha/beta oscillations and BOLD signals in the cortex to theta oscillations in the MTL. The results also demonstrate that decreases in theta power can index MTL involvement during encoding.Significance StatementStudies investigating the oscillatory correlates of memory encoding largely focus on activity in the theta frequency and often implicitly assume that increases in theta activity reflect similar processes as typically reported increases MTL activity changes in fMRI studies. The presented study found decreases in theta power, not increases, closely mapping to MTL BOLD signal increases during the same paradigm. This finding is in line with studies showing a negative relationship between low frequency power and BOLD changes in the cortex, but challenges the assumption that theta power increases reflect MTL activity. The reported findings importantly contribute to answer the question of how and which oscillatory activity indexes MTL memory processes.

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Representations of local spatial information in the human medial temporal lobe during memory-guided navigation

10.1101/2020.11.18.389346 ◽

2020 ◽

Author(s):

Shao-Fang Wang ◽

Valerie A. Carr ◽

Serra E. Favila ◽

Jeremy N. Bailenson ◽

Thackery I. Brown ◽

...

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Spatial Information ◽

Activity Patterns ◽

Critical Role ◽

Neural Representations ◽

Parahippocampal Cortex ◽

Pattern Similarity ◽

Cortical Regions ◽

Goal Directed Behavior

AbstractThe hippocampus (HC) and surrounding medial temporal lobe (MTL) cortical regions play a critical role in spatial navigation and episodic memory. However, it remains unclear how the interaction between the HC’s conjunctive coding and mnemonic differentiation contributes to neural representations of spatial environments. Multivariate functional magnetic resonance imaging (fMRI) analyses enable examination of how human HC and MTL cortical regions encode multidimensional spatial information to support memory-guided navigation. We combined high-resolution fMRI with a virtual navigation paradigm in which participants relied on memory of the environment to navigate to goal locations in two different virtual rooms. Within each room, participants were cued to navigate to four learned locations, each associated with one of two reward values. Pattern similarity analysis revealed that when participants successfully arrived at goal locations, activity patterns in HC and parahippocampal cortex (PHC) represented room-goal location conjunctions and activity patterns in HC subfields represented room-reward-location conjunctions. These results add to an emerging literature revealing hippocampal conjunctive representations during goal-directed behavior.

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Medial Prefrontal–Medial Temporal Theta Phase Coupling in Dynamic Spatial Imagery

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01064 ◽

2017 ◽

Vol 29 (3) ◽

pp. 507-519 ◽

Cited By ~ 15

Author(s):

Raphael Kaplan ◽

Daniel Bush ◽

James A. Bisby ◽

Aidan J. Horner ◽

Sofie S. Meyer ◽

...

Keyword(s):

Working Memory ◽

Temporal Lobe ◽

Medial Temporal Lobe ◽

Theta Rhythm ◽

Mental Simulation ◽

Retrosplenial Cortex ◽

Delay Period ◽

Phase Coupling ◽

Theta Phase ◽

Dynamic Imagery

Hippocampal–medial prefrontal interactions are thought to play a crucial role in mental simulation. Notably, the frontal midline/medial pFC (mPFC) theta rhythm in humans has been linked to introspective thought and working memory. In parallel, theta rhythms have been proposed to coordinate processing in the medial temporal cortex, retrosplenial cortex (RSc), and parietal cortex during the movement of viewpoint in imagery, extending their association with physical movement in rodent models. Here, we used noninvasive whole-head MEG to investigate theta oscillatory power and phase-locking during the 18-sec postencoding delay period of a spatial working memory task, in which participants imagined previously learned object sequences either on a blank background (object maintenance), from a first-person viewpoint in a scene (static imagery), or moving along a path past the objects (dynamic imagery). We found increases in 4- to 7-Hz theta power in mPFC when comparing the delay period with a preencoding baseline. We then examined whether the mPFC theta rhythm was phase-coupled with ongoing theta oscillations elsewhere in the brain. The same mPFC region showed significantly higher theta phase coupling with the posterior medial temporal lobe/RSc for dynamic imagery versus either object maintenance or static imagery. mPFC theta phase coupling was not observed with any other brain region. These results implicate oscillatory coupling between mPFC and medial temporal lobe/RSc theta rhythms in the dynamic mental exploration of imagined scenes.

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Theta Oscillations Mediate Interaction between Prefrontal Cortex and Medial Temporal Lobe in Human Memory

Cerebral Cortex ◽

10.1093/cercor/bhp223 ◽

2009 ◽

Vol 20 (7) ◽

pp. 1604-1612 ◽

Cited By ~ 123

Author(s):

Kristopher L. Anderson ◽

Rajasimhan Rajagovindan ◽

Georges A. Ghacibeh ◽

Kimford J. Meador ◽

Mingzhou Ding

Keyword(s):

Prefrontal Cortex ◽

Temporal Lobe ◽

Medial Temporal Lobe ◽

Human Memory ◽

Theta Oscillations

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Deep brain stimulation in the medial septum attenuates temporal lobe epilepsy via entrainment of hippocampal theta rhythm

CNS Neuroscience & Therapeutics ◽

10.1111/cns.13617 ◽

2021 ◽

Author(s):

Ying Wang ◽

Yating Shen ◽

Xianhui Cai ◽

Jie Yu ◽

Cong Chen ◽

...

Keyword(s):

Deep Brain Stimulation ◽

Temporal Lobe Epilepsy ◽

Temporal Lobe ◽

Brain Stimulation ◽

Theta Rhythm ◽

Medial Septum ◽

Hippocampal Theta Rhythm ◽

Hippocampal Theta ◽

Deep Brain

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The medial temporal lobe is critical for spatial relational perception

10.1101/765222 ◽

2019 ◽

Cited By ~ 1

Author(s):

Nicholas A. Ruiz ◽

Michael R. Meager ◽

Sachin Agarwal ◽

Mariam Aly

Keyword(s):

Temporal Lobe ◽

Medial Temporal Lobe ◽

Critical Role ◽

Long Term Memory ◽

Term Memory ◽

Cognitive Domains ◽

Attention Tasks ◽

Human Participants ◽

Attention And Perception

AbstractThe medial temporal lobe (MTL) is traditionally considered to be a system that is specialized for long-term memory. Recent work has challenged this notion by demonstrating that this region can contribute to many domains of cognition beyond long-term memory, including perception and attention. One potential reason why the MTL (and hippocampus specifically) contributes broadly to cognition is that it contains relational representations — representations of multidimensional features of experience and their unique relationship to one another — that are useful in many different cognitive domains. Here, we explore the hypothesis that the hippocampus/MTL plays a critical role in attention and perception via relational representations. We compared human participants with MTL damage to healthy age- and education-matched individuals on attention tasks that varied in relational processing demands. On each trial, participants viewed two images (rooms with paintings). On ‘similar room’ trials, they judged whether the rooms had the same spatial layout from a different perspective. On ‘similar art’ trials, they judged whether the paintings could have been painted by the same artist. On ‘identical’ trials, participants simply had to detect identical paintings or rooms. Patients were significantly and selectively impaired on the similar room task. This work provides further evidence that the hippocampus/MTL plays a ubiquitous role in cognition by virtue of its relational and spatial representations, and highlights its important contributions to rapid perceptual processes that benefit from attention.

Download Full-text