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

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.

2019 ◽  
Vol 116 (48) ◽  
pp. 24343-24352 ◽  
Author(s):  
Ethan A. Solomon ◽  
Bradley C. Lega ◽  
Michael R. Sperling ◽  
Michael J. Kahana

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.


2019 ◽  
Author(s):  
Zahra M. Aghajan ◽  
Diane Villaroman ◽  
Sonja Hiller ◽  
Tyler J. Wishard ◽  
Uros Topalovic ◽  
...  

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.


2017 ◽  
Author(s):  
Abhinav Goyal ◽  
Jonathan Miller ◽  
Andrew J. Watrous ◽  
Sang Ah Lee ◽  
Tom Coffey ◽  
...  

AbstractThe medial temporal lobe (MTL) is widely implicated in supporting episodic memory and navigation, but its precise functional role in organizing memory across time and space remains elusive. Here we examine the specific cognitive processes implemented by MTL structures (hippocampus and entorhinal cortex) to organize memory by using electrical brain stimulation, leveraging its ability to establish causal links between brain regions and features of behavior. We studied neurosurgical patients of both sexes who performed spatial-navigation and verbal-episodic memory tasks while brain stimulation was applied in various regions during learning. During the verbal memory task, stimulation in the MTL disrupted the temporal organization of encoded memories such that items learned with stimulation tended to be recalled in a more randomized order. During the spatial task, MTL stimulation impaired subjects’ abilities to remember items located far away from boundaries. These stimulation effects were specific to the MTL. Our findings thus provide the first causal demonstration in humans of the specific memory processes that are performed by the MTL to encode when and where events occurred.Significance StatementNumerous studies have implicated the medial temporal lobe (MTL) in encoding spatial and temporal memories, but they have not been able to causally demonstrate the nature of the cognitive processes by which this occurs in real-time. Electrical brain stimulation is able to demonstrate causal links between a brain region and a given function with high temporal precision. By examining behavior in a memory task as subjects received MTL stimulation, we provide the first causal evidence demonstrating the role of the MTL in organizing the spatial and temporal aspects of episodic memory.


2021 ◽  
pp. 174702182199382
Author(s):  
Dan PA Clark ◽  
Davide Bruno

There is disagreement in the literature as to whether episodic memory maintains an inherent temporal organisation, that is, whether learned items are necessarily organised along some temporal dimension or whether temporal organisation is a task-specific occurrence. The current series of experiments explored this issue. In Experiment 1, we tested whether temporal or spatial contiguity was present in an incidental encoding task where either strategy (but not both together) could be employed at test. In Experiment 2, we attempted to facilitate the use of a spatial retrieval strategy at test by asking participants to recall the location where target items had been displayed at study, after incidental encoding. Experiment 3 explored the role of study-test congruency by informing participants at encoding that they would be tested on either their memory for the temporal sequence or spatial locations, and then testing both at retrieval. Finally, Experiment 4 employed a masking task at encoding to ensure participants could not predict the true nature of the task, despite it being incidental, and a surprise free recall task. Predominantly, participants displayed recall performance consistent with temporal contiguity, although there was evidence for spatial contiguity under certain conditions. These results are consistent with the notion that episodic memory has a stable and predictable temporal organisation.


2018 ◽  
Author(s):  
Nora A. Herweg ◽  
Ashwini D. Sharan ◽  
Michael R. Sperling ◽  
Armin Brandt ◽  
Andreas Schulze-Bonhage ◽  
...  

AbstractThe medial temporal lobe (MTL) is known as the locus of spatial coding and episodic memory, but the interaction between these cognitive domains, as well as the extent to which they rely on common neurophysiological mechanisms is poorly understood. Here, we use a hybrid spatial-episodic memory task to determine how spatial information is dynamically reactivated in sub-regions of the MTL and how this reactivation guides recall of episodic information. Our results implicate theta oscillations across the MTL as a common neurophysiological substrate for spatial coding in navigation and episodic recall. We further show that spatial context information is initially retrieved in the hippocampus (HC) and subsequently emerges in the parahippocampal gyrus (PHG). Finally, we demonstrate that hippocampal theta phase modulates parahippocampal gamma amplitude during retrieval of spatial context, suggesting a role for cross frequency coupling in coding and transmitting retrieved spatial information.


2014 ◽  
Vol 369 (1635) ◽  
pp. 20130304 ◽  
Author(s):  
Joshua Jacobs

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.


Author(s):  
Ryoji Nishiyama ◽  
Jun Ukita

This study examined whether additional articulatory rehearsal induced temporary durability of phonological representations, using a 10-s delayed nonword free recall task. Three experiments demonstrated that cumulative rehearsal between the offset of the last study item and the start of the filled delay (Experiments 1 and 3) and a fixed rehearsal of the immediate item during the subsequent interstimulus interval (Experiments 2 and 3) improved free recall performance. These results suggest that an additional rehearsal helps to stabilize phonological representations for a short period. Furthermore, the analyses of serial position curves suggested that the frequency of the articulation affected the durability of the phonological representation. The significance of these findings as clues of the mechanism maintaining verbal information (i.e., verbal working memory) is discussed.


2020 ◽  
Author(s):  
Susan L. Benear ◽  
Elizabeth A. Horwath ◽  
Emily Cowan ◽  
M. Catalina Camacho ◽  
Chi Ngo ◽  
...  

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.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregory D. Clemenson ◽  
Antonella Maselli ◽  
Alexander J. Fiannaca ◽  
Amos Miller ◽  
Mar Gonzalez-Franco

AbstractGPS navigation is commonplace in everyday life. While it has the capacity to make our lives easier, it is often used to automate functions that were once exclusively performed by our brain. Staying mentally active is key to healthy brain aging. Therefore, is GPS navigation causing more harm than good? Here we demonstrate that traditional turn-by-turn navigation promotes passive spatial navigation and ultimately, poor spatial learning of the surrounding environment. We propose an alternative form of GPS navigation based on sensory augmentation, that has the potential to fundamentally alter the way we navigate with GPS. By implementing a 3D spatial audio system similar to an auditory compass, users are directed towards their destination without explicit directions. Rather than being led passively through verbal directions, users are encouraged to take an active role in their own spatial navigation, leading to more accurate cognitive maps of space. Technology will always play a significant role in everyday life; however, it is important that we actively engage with the world around us. By simply rethinking the way we interact with GPS navigation, we can engage users in their own spatial navigation, leading to a better spatial understanding of the explored environment.


2021 ◽  
Vol 11 (2) ◽  
pp. 162
Author(s):  
Aljoscha Thomschewski ◽  
Eugen Trinka ◽  
Julia Jacobs

The prefrontal cortex and hippocampus function in tight coordination during multiple cognitive processes. During spatial navigation, prefrontal neurons are linked to hippocampal theta oscillations, presumably in order to enhance communication. Hippocampal ripples have been suggested to reflect spatial memory processes. Whether prefrontal-hippocampal-interaction also takes place within the ripple band is unknown. This intracranial EEG study aimed to investigate whether ripple band coherences can also be used to show this communication. Twelve patients with epilepsy and intracranial EEG evaluation completed a virtual spatial navigation task. We calculated ordinary coherence between prefrontal and temporal electrodes during retrieval, re-encoding, and pre-task rest. Coherences were compared between the conditions via permutation testing. Additionally, ripples events were automatically detected and changes in occurrence rates were investigated excluding ripples on epileptic spikes. Ripple-band coherences yielded no general effect of the task on coherences across all patients. Furthermore, we did not find significant effects of task conditions on ripple rates. Subsequent analyses pointed to rather short periods of synchrony as opposed to general task-related changes in ripple-band coherence. Specifically designed tasks and adopted measures might be necessary in order to map these interactions in future studies.


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