scholarly journals Hippocampal theta sequences in REM sleep during spatial learning

2021 ◽  
Author(s):  
Mark C. Zielinski ◽  
Justin D. Shin ◽  
Shantanu P. Jadhav

ABSTRACTRapid eye movement (REM) sleep is known to play a role in hippocampally-dependent memory, yet the activity and development of hippocampal neuronal ensembles during this state is not well understood. Here we investigated patterning of CA1 place cell activity by theta oscillations, a shared electrophysiological hallmark of both waking behavior and REM sleep, in male rats learning a spatial memory task. We report the existence of REM theta sequences, sequential reactivations of place cells in REM theta that parallel waking theta sequences. REM and wake theta sequences develop rapidly with experience, recapitulating behavioral sequences of compressed space in forward and reverse directions throughout learning. REM sleep exhibited a balance of forward and reverse sequences in contrast to predominantly forward wake theta sequences. Finally, we found that a CA1 neuronal population known to shift preferred theta phases in REM exhibited differential participation in wake and REM theta sequences. In particular, this phase-shifting population showed an increased contribution to REM theta sequence representations after behavioral performance asymptotes and the task is learned, supporting a previously hypothesized role in depotentiation. These findings suggest a role for REM associated theta sequences in state dependent memory functions of the hippocampal circuit, providing evidence that REM sleep is associated with sequence reactivation that can support consolidation of representations necessary for memory guided behavior.

2019 ◽  
Author(s):  
Mark C. Zielinski ◽  
Justin D. Shin ◽  
Shantanu P. Jadhav

ABSTRACTInteractions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for memory-guided behavior. Theta oscillations (~8 Hz) underlie a key physiological mechanism for mediating these coordinated interactions, and theta oscillatory coherence and phase-locked spiking in the two regions have been shown to be important for spatial memory. Hippocampal place cell activity associated with theta oscillations encodes spatial position during behavior, and theta-phase associated spiking is known to further mediate a temporal code for space within CA1 place fields. Although prefrontal neurons are prominently phase-locked to hippocampal theta oscillations in spatial memory tasks, whether and how theta oscillations mediate processing of spatial information across these networks remains unclear. Here, we addressed these questions using simultaneous recordings of dorsal CA1 – PFC ensembles and population decoding analyses in male rats performing a continuous spatial working memory task known to require hippocampal-prefrontal interactions. We found that in addition to CA1, population activity in PFC can also encode the animal’s current spatial position on a theta-cycle timescale during memory-guided behavior. Coding of spatial position was coherent for CA1 and PFC ensembles, exhibiting correlated position representations within theta cycles. In addition, incorporating theta-phase information during decoding to account for theta-phase associated spiking resulted in a significant improvement in the accuracy of prefrontal spatial representations, similar to concurrent CA1 representations. These findings indicate a theta-oscillation mediated mechanism of temporal coordination for shared processing and communication of spatial information across the two networks during spatial memory-guided behavior.


1998 ◽  
Vol 274 (4) ◽  
pp. R1136-R1141 ◽  
Author(s):  
Richard L. Verrier ◽  
T. Rern Lau ◽  
Umesha Wallooppillai ◽  
James Quattrochi ◽  
Bruce D. Nearing ◽  
...  

Rapid eye movement (REM) sleep results in profound state-dependent alterations in heart rate. The present study describes a novel phenomenon of a primary deceleration in heart rate that is not preceded or followed by increases in heart rate or arterial blood pressure and occurs primarily during tonic REM sleep. The goals were to characterize the primary decelerations and to provide insights on the underlying central and peripheral autonomic mechanisms. Cats were chronically implanted with electrodes to record electroencephalogram, pontogeniculooccipital wave activity in lateral geniculate nucleus, hippocampal theta rhythm, electromyogram, electrooculogram, respiration (diaphragm), and electrocardiogram. Arterial blood pressure was monitored from a carotid artery catheter. R-R interval fluctuations were continuously tracked using customized software. The muscarinic blocking agent glycopyrrolate (0.1 mg/kg iv) and the β-adrenergic blocking agent atenolol (0.3 mg/kg iv) were administered in alternating sequence with a 90- to 120-min interval. Glycopyrrolate immediately eliminated the decelerations during REM sleep. Atenolol alone had no effect on their frequency. These findings suggest that a change in the centrally induced pattern of autonomic activity to the heart is responsible for the primary decelerations, namely, a bursting of cardiac vagal efferent fiber activity.


2019 ◽  
Author(s):  
Umesh Vivekananda ◽  
Daniel Bush ◽  
James A Bisby ◽  
Sallie Baxendale ◽  
Roman Rodionov ◽  
...  

AbstractHippocampal theta oscillations have been implicated in spatial memory function in both rodents and humans. What is less clear is how hippocampal theta interacts with higher frequency oscillations during spatial memory function, and how this relates to subsequent behaviour. Here we asked ten human epilepsy patients undergoing intracranial EEG recording to perform a desk-top virtual reality spatial memory task, and found that increased theta power in two discrete bands (‘low’ 2-5Hz and ‘high’ 6-9Hz) during cued retrieval was associated with improved task performance. Similarly, increased coupling between ‘low’ theta phase and gamma amplitude during the same period was associated with improved task performance. These results support a role of theta oscillations and theta-gamma phase-amplitude coupling in human spatial memory function.


2011 ◽  
Vol 106 (5) ◽  
pp. 2749-2763 ◽  
Author(s):  
Hao Zhang ◽  
Shih-Chieh Lin ◽  
Miguel A. L. Nicolelis

The medial septum-vertical limb of the diagonal band of Broca (MSvDB) is important for normal hippocampal functions and theta oscillations. Although many previous studies have focused on understanding how MSVDB neurons fire rhythmic bursts to pace hippocampal theta oscillations, a significant portion of MSVDB neurons are slow-firing and thus do not pace theta oscillations. The function of these MSVDB neurons, especially their role in modulating hippocampal activity, remains unknown. We recorded MSVDB neuronal ensembles in behaving rats, and identified a distinct physiologically homogeneous subpopulation of slow-firing neurons (overall firing <4 Hz) that shared three features: 1) much higher firing rate during rapid eye movement sleep than during slow-wave (SW) sleep; 2) temporary activation associated with transient arousals during SW sleep; 3) brief responses (latency 15∼30 ms) to auditory stimuli. Analysis of the fine temporal relationship of their spiking and theta oscillations showed that unlike the theta-pacing neurons, the firing of these “pro-arousal” neurons follows theta oscillations. However, their activity precedes short-term increases in hippocampal oscillation power in the theta and gamma range lasting for a few seconds. Together, these results suggest that these pro-arousal slow-firing MSvDB neurons may function collectively to promote hippocampal activation.


PLoS ONE ◽  
2009 ◽  
Vol 4 (4) ◽  
pp. e5238 ◽  
Author(s):  
Kafui Dzirasa ◽  
Lucas M. Santos ◽  
Sidarta Ribeiro ◽  
Jennifer Stapleton ◽  
Raul R. Gainetdinov ◽  
...  

2011 ◽  
Vol 122 (1) ◽  
pp. e5
Author(s):  
Jonathan Kleen ◽  
Barbara Jobst ◽  
Kandan Kulandaivel ◽  
Terrance Darcey ◽  
Gregory Holmes ◽  
...  

Author(s):  
Marcus O. Harrington ◽  
Scott A. Cairney

Abstract Purpose of Review Auditory stimulation is a technique that can enhance neural oscillations linked to overnight memory consolidation. In this review, we evaluate the impacts of auditory stimulation on the neural oscillations of sleep and associated memory processes in a variety of populations. Recent Findings Cortical EEG recordings of slow-wave sleep (SWS) are characterised by two cardinal oscillations: slow oscillations (SOs) and sleep spindles. Auditory stimulation delivered in SWS enhances SOs and phase-coupled spindle activity in healthy children and adults, children with ADHD, adults with mild cognitive impairment and patients with major depression. Under certain conditions, auditory stimulation bolsters the benefits of SWS for memory consolidation, although further work is required to fully understand the factors affecting stimulation-related memory gains. Recent work has turned to rapid eye movement (REM) sleep, demonstrating that auditory stimulation can be used to manipulate REM sleep theta oscillations. Summary Auditory stimulation enhances oscillations linked to overnight memory processing and shows promise as a technique for enhancing the memory benefits of sleep.


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