scholarly journals Ripple Band Phase Precession of Place Cell Firing during Replay

2021 ◽  
Author(s):  
Daniel Bush ◽  
Freyja Olafsdottir ◽  
Caswell Barry ◽  
Neil Burgess
Keyword(s):  
Hippocampal Formation ◽  
Receptive Fields ◽  
Negative Relationship ◽  
Place Cell ◽  
Place Cells ◽  
Phase Coding ◽  
Equivalent Rate ◽  
Phase Precession ◽  
Cell Firing ◽  
Ripple Phase

Phase coding offers several theoretical advantages for information transmission compared to an equivalent rate code. Phase coding is shown by place cells in the rodent hippocampal formation, which fire at progressively earlier phases of the movement related 6-12Hz theta rhythm as their spatial receptive fields are traversed. Importantly, however, phase coding is independent of carrier frequency, and so we asked whether it might also be exhibited by place cells during 150-250Hz ripple band activity, when they are thought to replay information to neocortex. We demonstrate that place cells which fire multiple spikes during candidate replay events do so at progressively earlier ripple phases, and that spikes fired across all replay events exhibit a negative relationship between decoded location within the firing field and ripple phase. These results provide insights into the mechanisms underlying phase coding and place cell replay, as well as the neural code propagated to downstream neurons.

scholarly journals Neural dynamics indicate parallel integration of environmental and self-motion information by place and grid cells

2019 ◽  
Author(s):  
Dmitri Laptev ◽  
Neil Burgess
Keyword(s):  
Path Integration ◽  
Temporal Dynamics ◽  
Hippocampal Formation ◽  
Place Cell ◽  
Place Cells ◽  
Motion Information ◽  
Grid Cells ◽  
Attractor Network ◽  
Cell Firing ◽  
Self Motion

AbstractPlace cells and grid cells in the hippocampal formation are thought to integrate sensory and self-motion information into a representation of estimated spatial location, but the precise mechanism is unknown. We simulated a parallel attractor system in which place cells form an attractor network driven by environmental inputs and grid cells form an attractor network performing path integration driven by self-motion, with inter-connections between them allowing both types of input to influence firing in both ensembles. We show that such a system is needed to explain the spatial patterns and temporal dynamics of place cell firing when rats run on a linear track in which the familiar correspondence between environmental and self-motion inputs is changed (Gothard et al., 1996b; Redish et al., 2000). In contrast, the alternative architecture of a single recurrent network of place cells (performing path integration and receiving environmental inputs) cannot reproduce the place cell firing dynamics. These results support the hypothesis that grid and place cells provide two different but complementary attractor representations (based on self-motion and environmental sensory inputs respectively). Our results also indicate the specific neural mechanism and main predictors of hippocampal map realignment and make predictions for future studies.

scholarly journals Theta phase precession of grid and place cell firing in open environments

2014 ◽  
Vol 369 (1635) ◽  
pp. 20120532 ◽  
Author(s):  
A. Jeewajee ◽  
C. Barry ◽  
V. Douchamps ◽  
D. Manson ◽  
C. Lever ◽  
...  
Keyword(s):  
Hippocampal Formation ◽  
Field Potential ◽  
Place Cells ◽  
Pool Data ◽  
Grid Cells ◽  
Phase Coding ◽  
Physiological Variables ◽  
Phase Precession ◽  
Field Peak ◽  
Theta Phase

Place and grid cells in the rodent hippocampal formation tend to fire spikes at successively earlier phases relative to the local field potential theta rhythm as the animal runs through the cell's firing field on a linear track. However, this ‘phase precession’ effect is less well characterized during foraging in two-dimensional open field environments. Here, we mapped runs through the firing fields onto a unit circle to pool data from multiple runs. We asked which of seven behavioural and physiological variables show the best circular–linear correlation with the theta phase of spikes from place cells in hippocampal area CA1 and from grid cells from superficial layers of medial entorhinal cortex. The best correlate was the distance to the firing field peak projected onto the animal's current running direction. This was significantly stronger than other correlates, such as instantaneous firing rate and time-in-field, but similar in strength to correlates with other measures of distance travelled through the firing field. Phase precession was stronger in place cells than grid cells overall, and robust phase precession was seen in traversals through firing field peripheries (although somewhat less than in traversals through the centre), consistent with phase coding of displacement along the current direction. This type of phase coding, of place field distance ahead of or behind the animal, may be useful for allowing calculation of goal directions during navigation.

scholarly journals Experience-dependent trends in CA1 theta and slow gamma rhythms in freely behaving mice

2018 ◽  
Vol 119 (2) ◽  
pp. 476-489 ◽  
Author(s):  
Brian J. Gereke ◽  
Alexandra J. Mably ◽  
Laura Lee Colgin
Keyword(s):  
Spatial Information ◽  
Hippocampal Formation ◽  
Cell Activity ◽  
Place Cell ◽  
Place Cells ◽  
Running Speed ◽  
Circular Track ◽  
Gamma Rhythms ◽  
Over Time ◽  
First Session

CA1 place cells become more anticipatory with experience, an effect thought to be caused by NMDA receptor-dependent plasticity in the CA3–CA1 network. Theta (~5–12 Hz), slow gamma (~25–50 Hz), and fast gamma (~50–100 Hz) rhythms are thought to route spatial information in the hippocampal formation and to coordinate place cell ensembles. Yet, it is unknown whether these rhythms exhibit experience-dependent changes concurrent with those observed in place cells. Slow gamma rhythms are thought to indicate inputs from CA3 to CA1, and such inputs are thought to be strengthened with experience. Thus, we hypothesized that slow gamma rhythms would become more evident with experience. We tested this hypothesis using mice freely traversing a familiar circular track for three 10-min sessions per day. We found that slow gamma amplitude was reduced in the early minutes of the first session of each day, even though both theta and fast gamma amplitudes were elevated during this same period. However, in the first minutes of the second and third sessions of each day, all three rhythms were elevated. Interestingly, theta was elevated to a greater degree in the first minutes of the first session than in the first minutes of later sessions. Additionally, all three rhythms were strongly influenced by running speed in dynamic ways, with the influence of running speed on theta and slow gamma changing over time within and across sessions. These results raise the possibility that experience-dependent changes in hippocampal rhythms relate to changes in place cell activity that emerge with experience. NEW & NOTEWORTHY We show that CA1 theta, slow gamma, and fast gamma rhythms exhibit characteristic changes over time within sessions in familiar environments. These effects in familiar environments evolve across repeated sessions.

scholarly journals Altered hippocampal place cell representation and theta rhythmicity following moderate prenatal alcohol exposure

2020 ◽  
Author(s):  
Ryan E. Harvey ◽  
Laura E. Berkowitz ◽  
Daniel D. Savage ◽  
Derek A. Hamilton ◽  
Benjamin J. Clark
Keyword(s):  
Spatial Memory ◽  
Prenatal Alcohol Exposure ◽  
Alcohol Exposure ◽  
Place Cell ◽  
Place Cells ◽  
Spatial Tuning ◽  
Cell Firing ◽  
Prenatal Alcohol ◽  
Ca3 Neurons ◽  
Hippocampal Place Cell

SummaryPrenatal alcohol exposure (PAE) leads to profound deficits in spatial memory and synaptic and cellular alterations to the hippocampus that last into adulthood. Neurons in the hippocampus, called place cells, discharge as an animal enters specific places in an environment, establish distinct ensemble codes for familiar and novel places, and are modulated by local theta rhythms. Spatial memory is thought to critically depend on the integrity of hippocampal place cell firing. We therefore tested the hypothesis that hippocampal place cell firing is impaired after PAE by performing in-vivo recordings from the hippocampi (CA1 and CA3) of moderate PAE and control adult rats. Our results show that hippocampal CA3 neurons from PAE rats have reduced spatial tuning. Secondly, CA1 and CA3 neurons from PAE rats are less likely to orthogonalize their firing between directions of travel on a linear track and between contexts in an open arena compared to control neurons. Lastly, reductions in the number of hippocampal place cells exhibiting significant theta rhythmicity and phase precession were observed which may suggest changes to hippocampal microcircuit function. Together, the reduced spatial tuning and sensitivity to context provides a neural systems-level mechanism to explain spatial memory impairment after moderate PAE.

scholarly journals Robotic and neuronal simulation of the hippocampus and rat navigation

1997 ◽  
Vol 352 (1360) ◽  
pp. 1535-1543 ◽  
Author(s):  
Neil Burgess ◽  
James G. Donnett ◽  
Kathryn J. Jeffery ◽  
John O–keefe
Keyword(s):  
Short Range ◽  
Place Cell ◽  
Place Cells ◽  
Proximity Data ◽  
Heading Direction ◽  
Cell Firing ◽  
Synaptic Changes ◽  
External Signals ◽  
Good Agreement

The properties of hippocampal place cells are reviewed, with particular attention to the nature of the internal and external signals that support their firing. A neuronal simulation of the firing of place cells in open–field environments of varying shape is presented. This simulation is coupled with an existing model of how place–cell firing can be used to drive navigation and is tested by implementation as a miniature mobile robot. The sensors on the robot provide visual, odometric and short–range proximity data, which are combined to estimate the distance of the walls of the enclosure from the robot and the robot's current heading direction. These inputs drive the hippocampal simulation, in which the robot's location is represented as the firing of place cells. If a goal location is encountered, learning occurs in connections from the concurrently active place cells to a set of ‘goal cells’, which guide subsequent navigation, allowing the robot to return to an unmarked location. The system shows good agreement with actual place–cell firing, and makes predictions regarding the firing of cells in the subiculum, the effect of blocking long–term synaptic changes, and the locus of search of rats after deformation of their environment.

scholarly journals Efficient phase coding in hippocampal place cells

2019 ◽  
Author(s):  
Pavithraa Seenivasan ◽  
Rishikesh Narayanan
Keyword(s):  
High Efficiency ◽  
Place Cells ◽  
Intrinsic Properties ◽  
Place Field ◽  
Phase Coding ◽  
Efficient Coding ◽  
Coding Efficiency ◽  
Synergistic Interactions ◽  
Phase Precession ◽  
Sequence Compression

ABSTRACTHippocampal place cells encode space through phase precession, whereby neuronal spike phase progressively advances during place-field traversals. What neural constraints are essential for achieving efficient transfer of information through such phase codes, while concomitantly maintaining signature neuronal excitability specific to individual cell types? We developed a conductance-based model for phase precession in CA1 pyramidal neurons within the temporal sequence compression framework, and defined phase-coding efficiency using information theory. We recruited an unbiased stochastic search strategy to build a model population that exhibited physiologically observed heterogeneities in intrinsic properties. Place-field responses elicited from these models matched signature sub- and supra-threshold place-cell characteristics, including phase precession, sub-threshold voltage ramps, increases in theta-frequency power and firing rate during place-field traversals. Employing this model population, we show that disparate parametric combinations with weak pair-wise correlations resulted in models with similar high-efficiency phase codes and similar excitability characteristics. Mechanistically, the emergence of such parametric degeneracy was dependent on the differential and variable impact of individual ion channels on phase-coding efficiency in different models, and importantly, on synergistic interactions between synaptic and intrinsic properties. Furthermore, our analyses predicted a dominant role for calcium-activated potassium channels in regulating phase precession and coding efficiency. Finally, change in afferent statistics, manifesting as input asymmetry, induced an adaptive shift in the phase code that preserved its efficiency, apart from introducing asymmetry in sub-threshold ramps and firing profiles during place-field traversals. Our study postulates degeneracy as a potential framework to attain the twin goals of efficient temporal coding and robust homeostasis.SIGNIFICANCE STATEMENTNeuronal intrinsic properties exhibit significant baseline heterogeneities, and change with activity-dependent plasticity and neuromodulation. How do hippocampal neurons encode spatial locations through the precise timings of their action potentials in the face of such heterogeneities? Here, employing a unifying synthesis of the temporal sequence compression, efficient coding and degeneracy frameworks, we show that there are several disparate routes for neurons to achieve high-efficiency spatial information transfer through such temporal codes. These disparate routes were consequent to the ability of neurons to produce precise encoding through distinct structural components, critically involving synergistic interactions between intrinsic and synaptic properties. Our results point to an explosion in the degrees of freedom available to a neuron in concomitantly achieving efficient coding and excitability homeostasis.

scholarly journals Variable place–cell coupling to a continuously viewed stimulus: evidence that the hippocampus is part of a perceptual system

1997 ◽  
Vol 352 (1360) ◽  
pp. 1505-1513 ◽  
Author(s):  
Alexander Rotenberg ◽  
Robert U. Muller
Keyword(s):  
Nervous System ◽  
Neural Activity ◽  
Angular Position ◽  
Place Cell ◽  
Place Cells ◽  
Perceptual System ◽  
Original Position ◽  
Cell Coupling ◽  
Mapping System ◽  
Cell Firing

A key feature of perception is that the interpretation of a single, continuously available stimulus can change from time to time. This aspect of perception is well illustrated by the use of ambiguous figures that can be seen in two different ways. When people view such a stimulus they almost universally describe what they are seeing as jumping between two states. If it is agreed that this perceptual phenemonon is causally linked to the activity of nerve cells, the state jumps would have to occur in conjunction with changes in neural activity somewhere in the nervous system. The experiments described in this paper suggest that hippocampal place cells are part of a perceptual system. Variations were made of a ‘cue–card rotation’ experiment on rats in which the angular position of a prominent visual stimulus on the wall of cylinder is changed in the rat's presence. The three main results are as follows. (i) Place–cell firing fields remain stationary if the cue is rotated by 180° so that the relation between the cue and the field is altered. (ii) Firing fields rotate by 45° when the cue is rotated by 45°and the relation between the field and the card is maintained. (iii) If the cue is first rotated by 180°and then rotated in a series of 45° steps, the field finishes at a different angular position relative to the card when the card is back in its original position. Thus, place cells can fire in two different ways in reponse to a continuously viewed stimulus. It is concluded that place cells reveal that the hippocampal mapping system also has properties expected of a perceptual system.

scholarly journals Spatial cell firing during virtual navigation of open arenas by head-restrained mice

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Guifen Chen ◽  
John Andrew King ◽  
Yi Lu ◽  
Francesca Cacucci ◽  
Neil Burgess
Keyword(s):  
Place Cell ◽  
Head Movements ◽  
Running Speed ◽  
Firing Patterns ◽  
Firing Rates ◽  
Theta Frequency ◽  
Phase Precession ◽  
Cell Firing ◽  
Theta Phase ◽  
Theta Phase Precession

We present a mouse virtual reality (VR) system which restrains head-movements to horizontal rotations, compatible with multi-photon imaging. This system allows expression of the spatial navigation and neuronal firing patterns characteristic of real open arenas (R). Comparing VR to R: place and grid, but not head-direction, cell firing had broader spatial tuning; place, but not grid, cell firing was more directional; theta frequency increased less with running speed, whereas increases in firing rates with running speed and place and grid cells' theta phase precession were similar. These results suggest that the omni-directional place cell firing in R may require local-cues unavailable in VR, and that the scale of grid and place cell firing patterns, and theta frequency, reflect translational motion inferred from both virtual (visual and proprioceptive) and real (vestibular translation and extra-maze) cues. By contrast, firing rates and theta phase precession appear to reflect visual and proprioceptive cues alone.

scholarly journals Place cells on a maze encode routes rather than destinations

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Roddy M Grieves ◽  
Emma R Wood ◽  
Paul A Dudchenko
Keyword(s):  
Place Cell ◽  
Place Cells ◽  
Spatial Discrimination ◽  
Goal Location ◽  
Cell Firing ◽  
Intended Destination ◽  
Start Location

Hippocampal place cells fire at different rates when a rodent runs through a given location on its way to different destinations. However, it is unclear whether such firing represents the animal’s intended destination or the execution of a specific trajectory. To distinguish between these possibilities, Lister Hooded rats (n = 8) were trained to navigate from a start box to three goal locations via four partially overlapping routes. Two of these led to the same goal location. Of the cells that fired on these two routes, 95.8% showed route-dependent firing (firing on only one route), whereas only two cells (4.2%) showed goal-dependent firing (firing similarly on both routes). In addition, route-dependent place cells over-represented the less discriminable routes, and place cells in general over-represented the start location. These results indicate that place cell firing on overlapping routes reflects the animal’s route, not its goals, and that this firing may aid spatial discrimination.

Sign in / Sign up

Export Citation Format

Share Document