scholarly journals Modulation of human intracranial theta oscillations during freely moving spatial navigation and memory

2019 ◽  
Author(s):  
Zahra M. Aghajan ◽  
Diane Villaroman ◽  
Sonja Hiller ◽  
Tyler J. Wishard ◽  
Uros Topalovic ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Spatial Memory ◽  
High Frequency ◽  
Medial Temporal Lobe ◽  
Spatial Navigation ◽  
Grid Cell ◽  
Cell System ◽  
Theta Oscillations ◽  
Neural Basis ◽  
Freely Moving

SummaryHow the human brain supports accurate navigation of a learned environment has been an active topic of research for nearly a century1–5. In rodents, the theta rhythm within the medial temporal lobe (MTL) has been proposed as a neural basis for fragmenting incoming information and temporally organizing experiences and is thus widely implicated in spatial and episodic memory6. In addition, high-frequency theta (~8Hz) is associated with navigation, and loss of theta results in spatial memory deficits in rats 7. Recently, high-frequency theta oscillations during ambulatory movement have been identified in humans8,9, though their relationship to spatial memory remains unexplored. Here, we were able to record MTL activity during spatial memory and navigation in freely moving humans immersed in a room-scale virtual reality (VR) environment. Naturalistic movements were captured using motion tracking combined with wireless VR in participants implanted with an intracranial electroencephalographic (iEEG) recording system for the treatment of epilepsy. We found that prevalence of theta oscillations across brain sites during both learning and recall of spatial locations during ambulatory navigation is critically linked to memory performance. This finding supports the reinstatement hypothesis of episodic memory—thought to underlie our ability to recreate a prior experience10–12—and suggests that theta prevalence within the MTL may act as a potential representational state for memory reinstatement during spatial navigation. Additionally, we found that theta power is hexadirectionally modulated13–15 as a function of the direction of physical movement, most prominently after learning has occurred. This effect bears a resemblance to the rodent grid cell system16 and suggests an analog in human navigation. Taken together, our results provide the first characterization of neural oscillations in the human MTL during ambulatory spatial memory tasks and provide a platform for future investigations of neural mechanisms underlying freely moving navigation in humans.

scholarly journals Hippocampal theta codes for distances in semantic and temporal spaces

2019 ◽  
Vol 116 (48) ◽  
pp. 24343-24352 ◽  
Author(s):  
Ethan A. Solomon ◽  
Bradley C. Lega ◽  
Michael R. Sperling ◽  
Michael J. Kahana
Keyword(s):  
Episodic Memory ◽  
Medial Temporal Lobe ◽  
Dynamic Range ◽  
Recall Performance ◽  
Spatial Navigation ◽  
Mapping Function ◽  
Cognitive Maps ◽  
Free Recall Task ◽  
Neurosurgical Patients ◽  
Hippocampal Theta

The medial temporal lobe (MTL) is known to support episodic memory and spatial navigation, raising the possibility that its true function is to form “cognitive maps” of any kind of information. Studies in humans and animals support the idea that the hippocampal theta rhythm (4 to 8 Hz) is key to this mapping function, as it has been repeatedly observed during spatial navigation tasks. If episodic memory and spatial navigation are 2 sides of the same coin, we hypothesized that theta oscillations might reflect relations between explicitly nonspatial items, such as words. We asked 189 neurosurgical patients to perform a verbal free-recall task, of which 96 had indwelling electrodes placed in the MTL. Subjects were instructed to remember short lists of sequentially presented nouns. We found that hippocampal theta power and connectivity during item retrieval coded for semantic distances between words, as measured using word2vec-derived subspaces. Additionally, hippocampal theta indexed temporal distances between words after filtering lists on recall performance, to ensure adequate dynamic range in time. Theta effects were noted only for semantic subspaces of 1 dimension, indicating a substantial compression of the possible semantic feature space. These results lend further support to our growing confidence that the MTL forms cognitive maps of arbitrary representational spaces, helping to reconcile longstanding differences between the spatial and episodic memory literatures.

scholarly journals Local generation of multineuronal spike sequences in the hippocampal CA1 region

2015 ◽  
Vol 112 (33) ◽  
pp. 10521-10526 ◽  
Author(s):  
Eran Stark ◽  
Lisa Roux ◽  
Ronny Eichler ◽  
György Buzsáki
Keyword(s):  
High Frequency ◽  
Single Neuron ◽  
Theta Oscillations ◽  
Ca1 Region ◽  
Hippocampal Ca1 Region ◽  
High Frequency Oscillations ◽  
Hippocampal Ca1 ◽  
Spike Sequences ◽  
Freely Moving ◽  
Local Generation

Sequential activity of multineuronal spiking can be observed during theta and high-frequency ripple oscillations in the hippocampal CA1 region and is linked to experience, but the mechanisms underlying such sequences are unknown. We compared multineuronal spiking during theta oscillations, spontaneous ripples, and focal optically induced high-frequency oscillations (“synthetic” ripples) in freely moving mice. Firing rates and rate modulations of individual neurons, and multineuronal sequences of pyramidal cell and interneuron spiking, were correlated during theta oscillations, spontaneous ripples, and synthetic ripples. Interneuron spiking was crucial for sequence consistency. These results suggest that participation of single neurons and their sequential order in population events are not strictly determined by extrinsic inputs but also influenced by local-circuit properties, including synapses between local neurons and single-neuron biophysics.

scholarly journals Neural basis of episodic memory in the intermediate term after medial temporal lobe resection

2019 ◽  
Vol 131 (3) ◽  
pp. 790-798 ◽  
Author(s):  
Woorim Jeong ◽  
Hyeongrae Lee ◽  
June Sic Kim ◽  
Chun Kee Chung
Keyword(s):  
Episodic Memory ◽  
Temporal Lobe ◽  
Verbal Memory ◽  
Visual Memory ◽  
Medial Temporal Lobe ◽  
Memory Performance ◽  
Memory Function ◽  
Memory Encoding ◽  
Neural Basis ◽  
Surgery Group

OBJECTIVEHow the brain supports intermediate-term preservation of memory in patients who have undergone unilateral medial temporal lobe resection (MTLR) has not yet been demonstrated. To understand the neural basis of episodic memory in the intermediate term after surgery for temporal lobe epilepsy (TLE), the authors investigated the relationship between the activation of the hippocampus (HIP) during successful memory encoding and individual memory capacity in patients who had undergone MTLR. They also compared hippocampal activation with other parameters, including structural volumes of the HIP, duration of illness, and age at seizure onset.METHODSThirty-five adult patients who had undergone unilateral MTLR at least 1 year before recruiting and who had a favorable seizure outcome were enrolled (17 left MTLR, 18 right MTLR; mean follow-up 6.31 ± 2.72 years). All patients underwent a standardized neuropsychological examination of memory function and functional MRI scanning with a memory-encoding paradigm of words and figures. Activations of the HIP during successful memory encoding were calculated and compared with standard neuropsychological memory scores, hippocampal volumes, and other clinical variables.RESULTSGreater activation in the HIP contralateral to the side of the resection was related to higher postoperative memory scores and greater postoperative memory improvement than the preoperative baseline in both patient groups. Specifically, postoperative verbal memory performance was positively correlated with contralateral right hippocampal activation during word encoding in the left-sided surgery group. In contrast, postoperative visual memory performance was positively correlated with contralateral left hippocampal activation during figure encoding in the right-sided surgery group. Activation of the ipsilateral remnant HIP was not correlated with any memory scores or volumes of the HIP; however, it had a negative correlation with the seizure-onset age and positive correlation with the duration of illness in both patient groups.CONCLUSIONSFor the first time, a neural basis that supports effective intermediate-term episodic memory after unilateral MTLR has been characterized. The results provide evidence that engagement of the HIP contralateral rather than ipsilateral to the side of resection is responsible for effective memory function in the intermediate term (> 1 year) after surgery in patients who have undergone left MTLR and right MTLR. Engagement of the material-specific contralesional HIP, verbal memory in the left-sided surgery group, and visual memory in the right-sided surgery group were observed.

scholarly journals Hippocampal theta codes for distances in semantic and temporal spaces

2019 ◽  
Author(s):  
Ethan A. Solomon ◽  
Bradley C. Lega ◽  
Michael R. Sperling ◽  
Michael J. Kahana
Keyword(s):  
Episodic Memory ◽  
Medial Temporal Lobe ◽  
Dynamic Range ◽  
Recall Performance ◽  
Spatial Navigation ◽  
Mapping Function ◽  
Cognitive Maps ◽  
Free Recall Task ◽  
Neurosurgical Patients ◽  
Hippocampal Theta

ABSTRACTThe medial temporal lobe (MTL) is known to support episodic memory and spatial navigation, raising the possibility that its true function is to form “cognitive maps” of any kind of information. Studies in humans and animals support the idea that the hippocampal theta rhythm (4-8 Hz) is key to this mapping function, as it has been repeatedly observed during spatial navigation tasks. If episodic memory and spatial navigation are two sides of the same coin, we hypothesized that theta oscillations would also reflect relations between explicitly nonspatial items, such as words. We asked 189 neurosurgical patients to perform a verbal free-recall task, of which 96 had indwelling electrodes placed in the MTL. Subjects were instructed to remember short lists of sequentially-presented nouns. We found that hippocampal theta power and connectivity during item retrieval coded for semantic distances between words, as measured using word2vec-derived subspaces. Additionally, hippocampal theta indexed temporal distances between words after filtering lists on recall performance, to ensure adequate dynamic range in time. Theta effects were only noted for semantic subspaces of 1-dimension, indicating a substantial compression of the possible semantic feature space. These results lend further support to our growing confidence that the MTL forms cognitive maps of arbitrary representational spaces, reconciling longstanding differences between the spatial and episodic memory literatures.

scholarly journals Development of Memory for Spatial Locations and Object/Place Associations in Infant Rhesus Macaques with and without Neonatal Hippocampal Lesions

2013 ◽  
Vol 19 (10) ◽  
pp. 1053-1064 ◽  
Author(s):  
Shala N. Blue ◽  
Andy M. Kazama ◽  
Jocelyne Bachevalier
Keyword(s):  
Spatial Memory ◽  
Medial Temporal Lobe ◽  
Time Course ◽  
Paired Comparison ◽  
Rhesus Macaques ◽  
Spatial Relations ◽  
Developmental Time ◽  
Neural Basis ◽  
Hippocampal Lesions ◽  
Spatial Locations

AbstractThis study traces the development of spatial memory abilities in monkeys and reports the effects of selective neonatal hippocampal lesions on performance across development. Two different versions of the visual paired-comparison (VPC) task were used. The VPC-Spatial-Location task tested memory for object-locations that could be solved using an egocentric spatial frame of reference and the VPC-Object-In-Place task taxed memory for spatial relations using an allocentric reference frame. Eleven rhesus macaques (6 neonatal sham-operated controls and 5 with neonatal neurotoxic hippocampal lesions) were tested on both tasks as infants (8 months), juveniles (18 months), and adults (5–6 years). Memory for spatial locations was present by 18 months of age, whereas memory for object-place relations was present only in adulthood. Also, neonatal hippocampal lesions delayed the emergence of memory for spatial locations and abolished memory for object-place associations, particularly in animals that had sustained extensive and bilateral hippocampal lesions. The differential developmental time course of spatial memory functions and of the effects of neonatal hippocampal lesions on these functions are discussed in relation to morphological maturation of the medial temporal lobe structures in monkeys. Implications of the findings for the neural basis of spatial memory development in humans are also considered. (JINS, 2013,19, 1–12)

scholarly journals Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory

2014 ◽  
Vol 369 (1635) ◽  
pp. 20130304 ◽  
Author(s):  
Joshua Jacobs
Keyword(s):  
Electrical Activity ◽  
Large Amplitude ◽  
Theta Rhythm ◽  
Spatial Navigation ◽  
Theta Oscillations ◽  
Mammalian Brain ◽  
Neural Basis ◽  
Human Hippocampus ◽  
Neurosurgical Patients ◽  
Hippocampal Theta

The theta oscillation is a neuroscience enigma. When a rat runs through an environment, large-amplitude theta oscillations (4–10 Hz) reliably appear in the hippocampus's electrical activity. The consistency of this pattern led to theta playing a central role in theories on the neural basis of mammalian spatial navigation and memory. However, in fact, hippocampal oscillations at 4–10 Hz are rare in humans and in some other species. This presents a challenge for theories proposing theta as an essential component of the mammalian brain, including models of place and grid cells. Here, I examine this issue by reviewing recent research on human hippocampal oscillations using direct brain recordings from neurosurgical patients. This work indicates that the human hippocampus does indeed exhibit rhythms that are functionally similar to theta oscillations found in rodents, but that these signals have a slower frequency of approximately 1–4 Hz. I argue that oscillatory models of navigation and memory derived from rodent data are relevant for humans, but that they should be modified to account for the slower frequency of the human theta rhythm.

Children show adult-like hippocampal pattern separation for familiar but not novel events

2020 ◽  
Author(s):  
Susan L. Benear ◽  
Elizabeth A. Horwath ◽  
Emily Cowan ◽  
M. Catalina Camacho ◽  
Chi Ngo ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Temporal Lobe ◽  
Medial Temporal Lobe ◽  
Developmental Change ◽  
Pattern Separation ◽  
Developmental Changes ◽  
Similarity Analysis ◽  
Separation Processes ◽  
Parahippocampal Cortex ◽  
Pattern Similarity

The medial temporal lobe (MTL) undergoes critical developmental change throughout childhood, which aligns with developmental changes in episodic memory. We used representational similarity analysis to compare neural pattern similarity for children and adults in hippocampus and parahippocampal cortex during naturalistic viewing of clips from the same movie or different movies. Some movies were more familiar to participants than others. Neural pattern similarity was generally lower for clips from the same movie, indicating that related content taxes pattern separation-like processes. However, children showed this effect only for movies with which they were familiar, whereas adults showed the effect consistently. These data suggest that children need more exposures to stimuli in order to show mature pattern separation processes.

Modulation of medial temporal lobe activity in epilepsy patients with hippocampal sclerosis during verbal working memory

2009 ◽  
Vol 15 (4) ◽  
pp. 536-546 ◽  
Author(s):  
PABLO CAMPO ◽  
FERNANDO MAESTÚ ◽  
IRENE GARCÍA-MORALES ◽  
ANTONIO GIL-NAGEL ◽  
BRYAN STRANGE ◽  
...  
Keyword(s):  
Working Memory ◽  
Episodic Memory ◽  
Temporal Lobe ◽  
Medial Temporal Lobe ◽  
Time Course ◽  
Hippocampal Sclerosis ◽  
Stimulus Presentation ◽  
Verbal Working Memory ◽  
Compelling Evidence ◽  
Electrophysiological Studies

AbstractIt has been traditionally assumed that medial temporal lobe (MTL) is not required for working memory (WM). However, animal lesion and electrophysiological studies and human neuropsychological and neuroimaging studies have provided increasing evidences of a critical involvement of MTL in WM. Based on previous findings, the central aim of this study was to investigate the contribution of the MTL to verbal WM encoding. Here, we used magnetoencephalography (MEG) to compare the patterns of MTL activation of 9 epilepsy patients suffering from left hippocampal sclerosis with those of 10 healthy matched controls while they performed a verbal WM task. MEG recordings allow detailed tracking of the time course of MTL activation. We observed impaired WM performance associated with changes in the dynamics of MTL activity in epilepsy patients. Specifically, whereas patients showed decreased activity in damaged MTL, activity in the contralateral MTL was enhanced, an effect that became significant in the 600- to 700-ms interval after stimulus presentation. These findings strongly support the crucial contribution of MTL to verbal WM encoding and provide compelling evidence for the proposal that MTL contributes to both episodic memory and WM. Whether this pattern is signaling reorganization or a normal use of a damaged structure is discussed. (JINS, 2009, 15, 536–546.)

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