scholarly journals Alternating sequences of future and past behavior encoded within hippocampal theta oscillations

Science ◽  
2020 ◽  
Vol 370 (6513) ◽  
pp. 247-250 ◽  
Author(s):  
Mengni Wang ◽  
David J. Foster ◽  
Brad E. Pfeiffer
Keyword(s):  
Activity Patterns ◽  
Place Cells ◽  
Theta Oscillations ◽  
Retrospective Evaluation ◽  
Past Behavior ◽  
Hippocampal Ca1 ◽  
Ongoing Behavior ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
And Storage

Neural networks display the ability to transform forward-ordered activity patterns into reverse-ordered, retrospective sequences. The mechanisms underlying this transformation remain unknown. We discovered that, during active navigation, rat hippocampal CA1 place cell ensembles are inherently organized to produce independent forward- and reverse-ordered sequences within individual theta oscillations. This finding may provide a circuit-level basis for retrospective evaluation and storage during ongoing behavior. Theta phase procession arose in a minority of place cells, many of which displayed two preferred firing phases in theta oscillations and preferentially participated in reverse replay during subsequent rest. These findings reveal an unexpected aspect of theta-based hippocampal encoding and provide a biological mechanism to support the expression of reverse-ordered sequences.

scholarly journals Prefrontal cortical activity predicts the extra-place field spiking of hippocampal place cells

2020 ◽  
Author(s):  
Jai Y. Yu ◽  
Loren M. Frank
Keyword(s):  
Receptive Field ◽  
Receptive Fields ◽  
Cortical Activity ◽  
Place Cells ◽  
Theta Oscillations ◽  
Place Field ◽  
Prefrontal Cortical ◽  
Hippocampal Ca1 ◽  
Non Local ◽  
Hippocampal Theta

AbstractThe receptive field of a neuron describes the regions of a stimulus space where the neuron is consistently active. Sparse spiking outside of the receptive field is often considered to be noise, rather than a reflection of information processing. Whether this characterization is accurate remains unclear. We therefore contrasted the sparse, temporally isolated spiking of hippocampal CA1 place cells to the consistent, temporally adjacent spiking seen within their spatial receptive fields (“place fields”). We found that isolated spikes, which occur during locomotion, are more strongly phase coupled to hippocampal theta oscillations than adjacent spikes and, surprisingly, transiently express coherent representations of non-local spatial representations. Further, prefrontal cortical activity is coordinated with, and can predict the occurrence of future isolated spiking events. Rather than local noise within the hippocampus, sparse, isolated place cell spiking reflects a coordinated cortical-hippocampal process consistent with the generation of non-local scenario representations during active navigation.

scholarly journals Prefrontal cortical activity predicts the occurrence of nonlocal hippocampal representations during spatial navigation

PLoS Biology ◽  
2021 ◽  
Vol 19 (9) ◽  
pp. e3001393
Author(s):  
Jai Y. Yu ◽  
Loren M. Frank
Keyword(s):  
Receptive Field ◽  
Receptive Fields ◽  
Cortical Activity ◽  
Place Cells ◽  
Theta Oscillations ◽  
Spatial Representations ◽  
Stimulus Space ◽  
Prefrontal Cortical ◽  
Hippocampal Ca1 ◽  
Hippocampal Theta

The receptive field of a neuron describes the regions of a stimulus space where the neuron is consistently active. Sparse spiking outside of the receptive field is often considered to be noise, rather than a reflection of information processing. Whether this characterization is accurate remains unclear. We therefore contrasted the sparse, temporally isolated spiking of hippocampal CA1 place cells to the consistent, temporally adjacent spiking seen within their spatial receptive fields (“place fields”). We found that isolated spikes, which occur during locomotion, are strongly phase coupled to hippocampal theta oscillations and transiently express coherent nonlocal spatial representations. Further, prefrontal cortical activity is coordinated with and can predict the occurrence of future isolated spiking events. Rather than local noise within the hippocampus, sparse, isolated place cell spiking reflects a coordinated cortical–hippocampal process consistent with the generation of nonlocal scenario representations during active navigation.

scholarly journals Behavior-dependent spatial maps enable efficient theta phase coding

2021 ◽  
Author(s):  
Eloy Parra-Barrero ◽  
Kamran Diba ◽  
Sen Cheng
Keyword(s):  
Place Cells ◽  
Spatial Representations ◽  
Place Field ◽  
Phase Code ◽  
Phase Precession ◽  
Relevant Variables ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
Exact Relationship ◽  
Speed Characteristic

AbstractNavigation through space involves learning and representing relationships between past, current and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations start behind the animal’s location and then sweep forward. However, the exact relationship between phase and represented and true positions remains unclear and even paradoxical. Here, we formalize previous notions as ‘spatial’ or ‘temporal’ sweeps, analyze single-cell and population variables in recordings from rat CA1 place cells, and compare them to model simulations. We show that neither sweep type quantitatively accounts for all relevant variables. Thus we introduce ‘behavior-dependent’ sweeps, which fit our key observation that sweep length, and hence place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. This structured heterogeneity is essential for understanding the hippocampal code.

Oscillator-Interference Models of Path Integration Do Not Require Theta Oscillations

2015 ◽  
Vol 27 (3) ◽  
pp. 548-560 ◽  
Author(s):  
Jeff Orchard
Keyword(s):  
Path Integration ◽  
Activity Patterns ◽  
Field Potential ◽  
Grid Cell ◽  
Place Cells ◽  
Theta Oscillations ◽  
Grid Cells ◽  
Neural Oscillators ◽  
Theta Frequency ◽  
Interference Models

Navigation and path integration in rodents seems to involve place cells, grid cells, and theta oscillations (4–12 Hz) in the local field potential. Two main theories have been proposed to explain the neurological underpinnings of how these phenomena relate to navigation and to each other. Attractor network (AN) models revolve around the idea that local excitation and long-range inhibition connectivity can spontaneously generate grid-cell-like activity patterns. Oscillator interference (OI) models propose that spatial patterns of activity are caused by the interference patterns between neural oscillators. In rats, these oscillators have a frequency close to the theta frequency. Recent studies have shown that bats do not exhibit a theta cycle when they crawl, and yet they still have grid cells. This has been interpreted as a criticism of OI models. However, OI models do not require theta oscillations. We explain why the absence of theta oscillations does not contradict OI models and discuss how the two families of models might be distinguished experimentally.

scholarly journals Modulation of visual cortex by hippocampal signals

2019 ◽  
Author(s):  
Julien Fournier ◽  
Aman B Saleem ◽  
E Mika Diamanti ◽  
Miles J Wells ◽  
Kenneth D Harris ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Sensory Processing ◽  
Visual Cues ◽  
Physical Distance ◽  
Place Cells ◽  
Theta Oscillations ◽  
Spatial Representations ◽  
Ca1 Neurons ◽  
V1 Neurons ◽  
Hippocampal Theta

Neurons in primary visual cortex (V1) are influenced by the animal’s position in the environment and encode positions that correlate with those encoded by hippocampus (CA1). Might V1’s encoding of spatial positions be inherited from hippocampal regions? If so, it should depend on non-visual factors that affect the encoding of position in hippocampus, such as the physical distance traveled and the phase of theta oscillations. We recorded V1 and CA1 neurons while mice ran through a virtual corridor and confirmed these predictions. Spatial representations in V1 and CA1 were correlated even in the absence of visual cues. Moreover, similar to CA1 place cells, the spatial responses of V1 neurons were influenced by the physical distance traveled and the phase of hippocampal theta oscillations. These results reveal a modulation of cortical sensory processing by non-sensory estimates of position that might originate in hippocampal regions.

scholarly journals Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jai Y Yu ◽  
Kenneth Kay ◽  
Daniel F Liu ◽  
Irene Grossrubatscher ◽  
Adrianna Loback ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Neural Activity ◽  
Spatial Representation ◽  
Spatial Navigation ◽  
Activity Patterns ◽  
Place Cells ◽  
Neural Mechanisms ◽  
Continuous Representation ◽  
Hippocampal Ca1 ◽  
Memory Representations

While ongoing experience proceeds continuously, memories of past experience are often recalled as episodes with defined beginnings and ends. The neural mechanisms that lead to the formation of discrete episodes from the stream of neural activity patterns representing ongoing experience are unknown. To investigate these mechanisms, we recorded neural activity in the rat hippocampus and prefrontal cortex, structures critical for memory processes. We show that during spatial navigation, hippocampal CA1 place cells maintain a continuous spatial representation across different states of motion (movement and immobility). In contrast, during sharp-wave ripples (SWRs), when representations of experience are transiently reactivated from memory, movement- and immobility-associated activity patterns are most often reactivated separately. Concurrently, distinct hippocampal reactivations of movement- or immobility-associated representations are accompanied by distinct modulation patterns in prefrontal cortex. These findings demonstrate a continuous representation of ongoing experience can be separated into independently reactivated memory representations.

Analysis of Recordings of Single-Unit Firing and Population Activity in the Dorsal Subiculum of Unrestrained, Freely Moving Rats

2003 ◽  
Vol 90 (2) ◽  
pp. 655-665 ◽  
Author(s):  
Michael I. Anderson ◽  
Shane M. O'Mara
Keyword(s):  
Neuronal Activity ◽  
Hippocampal Formation ◽  
Theta Oscillations ◽  
Population Activity ◽  
Male Adult ◽  
Sharp Waves ◽  
Hippocampal Ca1 ◽  
Ongoing Behavior ◽  
Restricted Environment ◽  
Fast Spiking

We examined neuronal activity in the dorsal subiculum of unrestrained, male adult Wistar rats, which were implanted with a moveable eight-electrode microdrive. The subiculum is the primary hippocampal formation output area and is comparatively uninvestigated neurophysiologically. We compared subicular unit activity and the subicular EEG while rats occupied a small, restricted environment and also correlated neuronal activity with the ongoing behavior of the animal. Units were separated using their electrophysiological characteristics into bursting units, regular spiking units, theta-modulated units, and fast spiking units. The bursting and regular spiking unit classes are similar to hippocampal CA1 units, whereas the fast spiking units appear to be interneurons. Bursting units were variable in their behavior: some units bursted regularly, and others bursted only occasionally. Theta-modulated units have not been described before; these were similar to regular spiking units in all respects except that they increased their firing significantly when theta oscillations were present in the simultaneous EEG record. Subicular EEG was similar to hippocampal EEG, with theta oscillations dominating “alert, moving” behaviors, while large amplitude irregular activity (LIA), which included sharp waves, predominated when theta oscillations were not present, mainly during “alert, still” and “quiet” behaviors. A relatively small proportion of subicular recordings (approximately 32%) were phase-locked to theta; this is a smaller proportion than in areas from which the subiculum takes major inputs. The relative lack of entrainment of subicular neurons by this important intrinsic rhythm is suggestive of a limit to which theta might be capable of affecting both subicular and hippocampal information processing more generally.

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