Hippocampal place cells use vector computations to navigate

Mapping Intimacies ◽

10.1101/2021.06.23.449621 ◽

2021 ◽

Author(s):

Jake Ormond ◽

John O'Keefe

Keyword(s):

Spatial Representation ◽

Vector Fields ◽

Cell Activity ◽

Choice Point ◽

Place Cell ◽

Place Cells ◽

Population Vector ◽

Goal Location ◽

Optimal Paths ◽

Independent Assessment

One function of the Hippocampal Cognitive Map is to provide information about salient locations in familiar environments such as those containing reward or danger, and to support navigation towards or away from those locations. Although much is known about how the hippocampus encodes location in world-centred coordinates, how it supports flexible navigation is less well understood. We recorded from CA1 place cells while rats navigated to a goal or freely foraged on the honeycomb maze. The maze tests the animal's ability to navigate using indirect as well as direct paths to the goal and allows the directionality of place cells to be assessed at each choice point during traversal to the goal. Place fields showed strong directional polarization in the navigation task, and to a lesser extent during random foraging. This polarization was characterized by vector fields which converged to sinks distributed throughout the environment. The distribution of these convergence sinks was centred near the goal location, and the population vector field converged on the goal, providing a strong navigational signal. Changing the goal location led to the movement of ConSinks and vector fields towards the new goal and within-days, the ConSink distance to the goal decreased with continued training. The honeycomb maze allows the independent assessment of spatial representation and spatial action in place cell activity and shows how the latter depends on the former. The results suggest a vector-based model of how the hippocampus supports flexible navigation, allowing animals to select optimal paths to destinations from any location in the environment.

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

Journal of Neurophysiology ◽

10.1152/jn.00472.2017 ◽

2018 ◽

Vol 119 (2) ◽

pp. 476-489 ◽

Cited By ~ 4

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.

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Representation of Objects in Space by Two Classes of Hippocampal Pyramidal Cells

The Journal of General Physiology ◽

10.1085/jgp.200409015 ◽

2004 ◽

Vol 124 (1) ◽

pp. 9-25 ◽

Cited By ~ 55

Author(s):

Bruno Rivard ◽

Yu Li ◽

Pierre-Pascal Lenck-Santini ◽

Bruno Poucet ◽

Robert U. Muller

Keyword(s):

Cell Activity ◽

Pyramidal Cells ◽

Place Cell ◽

Place Cells ◽

Rat Hippocampus ◽

Ca1 Pyramidal Cells ◽

New Class ◽

Familiar Environment ◽

Current Arrangement ◽

Number Of Cells

Humans can recognize and navigate in a room when its contents have been rearranged. Rats also adapt rapidly to movements of objects in a familiar environment. We therefore set out to investigate the neural machinery that underlies this capacity by further investigating the place cell–based map of the surroundings found in the rat hippocampus. We recorded from single CA1 pyramidal cells as rats foraged for food in a cylindrical arena (the room) containing a tall barrier (the furniture). Our main finding is a new class of cells that signal proximity to the barrier. If the barrier is fixed in position, these cells appear to be ordinary place cells. When, however, the barrier is moved, their activity moves equally and thereby conveys information about the barrier's position relative to the arena. When the barrier is removed, such cells stop firing, further suggesting they represent the barrier. Finally, if the barrier is put into a different arena where place cell activity is changed beyond recognition (“remapping”), these cells continue to discharge at the barrier. We also saw, in addition to barrier cells and place cells, a small number of cells whose activity seemed to require the barrier to be in a specific place in the environment. We conclude that barrier cells represent the location of the barrier in an environment-specific, place cell framework. The combined place + barrier cell activity thus mimics the current arrangement of the environment in an unexpectedly realistic fashion.

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Reconceiving the hippocampal map as a topological template

eLife ◽

10.7554/elife.03476 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 59

Author(s):

Yuri Dabaghian ◽

Vicky L Brandt ◽

Loren M Frank

Keyword(s):

Computational Model ◽

Spatial Cognition ◽

Cell Activity ◽

Place Cell ◽

Higher Order ◽

Place Cells ◽

Wide Range ◽

New Directions ◽

Place Fields

The role of the hippocampus in spatial cognition is incontrovertible yet controversial. Place cells, initially thought to be location-specifiers, turn out to respond promiscuously to a wide range of stimuli. Here we test the idea, which we have recently demonstrated in a computational model, that the hippocampal place cells may ultimately be interested in a space's topological qualities (its connectivity) more than its geometry (distances and angles); such higher-order functioning would be more consistent with other known hippocampal functions. We recorded place cell activity in rats exploring morphing linear tracks that allowed us to dissociate the geometry of the track from its topology. The resulting place fields preserved the relative sequence of places visited along the track but did not vary with the metrical features of the track or the direction of the rat's movement. These results suggest a reinterpretation of previous studies and new directions for future experiments.

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Place cells on a maze encode routes rather than destinations

eLife ◽

10.7554/elife.15986 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 40

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.

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Theta-modulation drives the emergence of network-wide connectivity patterns underlying replay in a model of hippocampal place cells

10.1101/118489 ◽

2017 ◽

Cited By ~ 1

Author(s):

Panagiota Theodoni ◽

Bernat Rovira ◽

Yingxue Wang ◽

Alex Roxin

Keyword(s):

Cell Activity ◽

Pyramidal Cells ◽

Spatial Location ◽

Medial Septum ◽

Place Cell ◽

Place Cells ◽

Synaptic Connectivity ◽

Pairwise Correlation ◽

Ca1 Pyramidal Cells ◽

Spatial Environment

SummaryPlace cells of the rodent hippocampus fire action potentials when the animal traverses a particular spatial location in a given environment. Therefore, for any given trajectory one will observe a repeatable sequence of place cell activations as the animal explores. Interestingly, when the animal is quiescent or sleeping, one can observe similar sequences of activation, although at a highly compressed rate, known as “replays”. It is hypothesized that this replay underlies the process of memory consolidation whereby memories are “transferred” from hippocampus to cortex. However, it remains unclear how the memory of a particular environment is actually encoded in the place cell activity and what the mechanism for replay is. Here we study how plasticity during spatial exploration shapes the patterns of synaptic connectivity in model networks of place cells. Specifically, we show how plasticity leads to the emergence of patterns of activity which represent the spatial environment learned. These states become spontaneously active when the animal is quiescent, reproducing the phenomenology of replays. Interestingly, replay emerges most rapidly when place cell activity is modulated by an ongoing oscillation. The optimal oscillation frequency can be calculated analytically, is directly related to the plasticity rule, and for experimentally determined values of the plasticity window in rodent slices gives values in the theta range. A major prediction of this model is that the pairwise correlation of place cells which encode for neighboring locations should increase during initial exploration, leading up to the critical transition. We find such an increase in a population of simultaneously recorded CA1 pyramidal cells from a rat exploring a novel track. Furthermore, in a rat in which hippocampal theta is reduced through inactivation of the medial septum we find no such increase. Our model is the first to show how theta-modulation can speed up learning by facilitating the emergence of environment-specific network-wide patterns of synaptic connectivity in hippocampal circuits.

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Coordinated emergence of hippocampal replay and theta sequences during post-natal development

10.1101/505636 ◽

2018 ◽

Author(s):

Laurenz Muessig ◽

Michal Lasek ◽

Isabella Varsavsky ◽

Francesca Cacucci ◽

Thomas J Wills

Keyword(s):

Cell Activity ◽

Place Cell ◽

Place Cells ◽

Network Activity ◽

Recent Experience ◽

Sequence Generation ◽

Late Emergence ◽

Current Location ◽

Cell Firing ◽

Dependent Learning

Hippocampal place cells encode an animal's current position in space during exploration. During subsequent sleep, hippocampal network activity recapitulates patterns observed during recent experience: place cells with overlapping spatial firing fields during locomotion show a greater tendency to co-fire ("reactivation") and temporally ordered and compressed sequences of place cell firing observed during wakefulness are reinstated ("replay"). Reactivation and replay are thought to be network mechanisms underlying memory consolidation. Compressed sequences of place cell firing also occur during exploration: during each cycle of the theta oscillation, the set of active place cells shifts from those signalling positions behind to those signalling positions ahead of an animal's current location. These "theta sequences" have been linked to spatial planning. Here we demonstrate that, before weaning (post-natal day 21, P21), offline place cell activity reflects predominantly stationary locations in recently visited environments. By contrast, sequential place cell firing, describing extended trajectories through space during exploration ("theta sequences") and subsequent sleep ("replay"), emerge gradually after weaning in a coordinated fashion, possibly due to a protracted decrease in the threshold for experience-driven plasticity. Hippocampus-dependent learning and memory emerge late in altricial mammals, appearing around weaning in rats and slowly maturing thereafter. In contrast, spatially localised firing can be observed at least one week earlier (albeit with reduced spatial tuning/stability). By examining the emergence of hippocampal reactivation, replay, and theta sequences during development, we show that the coordinated maturation of offline consolidation and online sequence generation parallels the late emergence of hippocampal memory in the rat.

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Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior

eLife ◽

10.7554/elife.08902 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 35

Author(s):

Daniel Christopher Haggerty ◽

Daoyun Ji

Keyword(s):

Cortical Neurons ◽

Specific Activity ◽

Cell Activity ◽

Place Cell ◽

Place Cells ◽

Spatial Behavior ◽

Freely Moving Rats ◽

Freely Moving ◽

Visual Cortical ◽

Hippocampal Place Cell

Visual cues exert a powerful control over hippocampal place cell activities that encode external spaces. The functional interaction of visual cortical neurons and hippocampal place cells during spatial navigation behavior has yet to be elucidated. Here we show that, like hippocampal place cells, many neurons in the primary visual cortex (V1) of freely moving rats selectively fire at specific locations as animals run repeatedly on a track. The V1 location-specific activity leads hippocampal place cell activity both spatially and temporally. The precise activities of individual V1 neurons fluctuate every time the animal travels through the track, in a correlated fashion with those of hippocampal place cells firing at overlapping locations. The results suggest the existence of visual cortical neurons that are functionally coupled with hippocampal place cells for spatial processing during natural behavior. These visual neurons may also participate in the formation and storage of hippocampal-dependent memories.

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Defective place cell activity in nociceptin receptor knockout mice with elevated NMDA receptor-dependent long-term potentiation

The Journal of Physiology ◽

10.1113/jphysiol.2004.081802 ◽

2005 ◽

Vol 565 (2) ◽

pp. 579-591 ◽

Cited By ~ 14

Author(s):

Franco A. Taverna ◽

John Georgiou ◽

Robert J. McDonald ◽

Nancy S. Hong ◽

Alexander Kraev ◽

...

Keyword(s):

Nmda Receptor ◽

Knockout Mice ◽

Cell Activity ◽

Long Term Potentiation ◽

Place Cell ◽

Term Potentiation ◽

Nociceptin Receptor

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Hippocampal Place-Cell Firing During Movement in Three-Dimensional Space

Journal of Neurophysiology ◽

10.1152/jn.2001.85.1.105 ◽

2001 ◽

Vol 85 (1) ◽

pp. 105-116 ◽

Cited By ~ 44

Author(s):

James J. Knierim ◽

Bruce L. McNaughton

Keyword(s):

Hippocampal Neurons ◽

Horizontal Plane ◽

Three Dimensional ◽

Place Cell ◽

Place Cells ◽

Limbic Cortex ◽

Head Direction ◽

Head Direction Cells ◽

Recording Apparatus ◽

Place Fields

“Place” cells of the rat hippocampus are coupled to “head direction” cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45° generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their “tuning functions” in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.

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