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

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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Manipulating Hippocampal Place Cell Activity by Single-Cell Stimulation in Freely Moving Mice

Cell Reports ◽

10.1016/j.celrep.2018.03.031 ◽

2018 ◽

Vol 23 (1) ◽

pp. 32-38 ◽

Cited By ~ 22

Author(s):

Maria Diamantaki ◽

Stefano Coletta ◽

Khaled Nasr ◽

Roxana Zeraati ◽

Sophie Laturnus ◽

...

Keyword(s):

Single Cell ◽

Cell Activity ◽

Place Cell ◽

Cell Stimulation ◽

Freely Moving ◽

Hippocampal Place Cell

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Place cell firing cannot support navigation without intact septal circuits

10.1101/470088 ◽

2018 ◽

Cited By ~ 3

Author(s):

Kevin A. Bolding ◽

Janina Ferbinteanu ◽

Steven E. Fox ◽

Robert U. Muller

Keyword(s):

Specific Activity ◽

Cell Activity ◽

Normal Activity ◽

Medial Septum ◽

Place Cell ◽

Spatial Behavior ◽

Oscillatory Activity ◽

Gaba A ◽

Definitive Answer ◽

Hippocampal Theta

Though it has been known for over half a century that interference with the normal activity of septohippocampal neurons can abolish hippocampal theta rhythmicity, a definitive answer to the question of its function has remained elusive. To clarify the role of septal circuits and theta in location specific activity of place cells and spatial behavior, three drugs were delivered to the medial septum of rats: tetracaine, a local anesthetic; muscimol, a GABA-A agonist; and gabazine, a GABA-A antagonist. All three drugs disrupted normal oscillatory activity in the hippocampus. However, tetracaine and muscimol both reduced spatial firing and interfered with the rat’s ability to navigate to a hidden goal. After gabazine, location specific firing was preserved in the absence of theta, but rats were unable to accurately locate the hidden goal. These results indicate that theta is unnecessary for location specific firing of hippocampal cells, and that place cell activity cannot support accurate navigation when septal circuits are disrupted.

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

10.7554/elife.08902.017 ◽

2015 ◽

Keyword(s):

Hippocampal Neurons ◽

Spatial Behavior ◽

Freely Moving Rats ◽

Freely Moving ◽

Visual Cortical

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

10.7554/elife.08902.018 ◽

2015 ◽

Cited By ~ 1

Author(s):

Daniel Christopher Haggerty ◽

Daoyun Ji

Keyword(s):

Hippocampal Neurons ◽

Spatial Behavior ◽

Author Response ◽

Freely Moving Rats ◽

Freely Moving ◽

Visual Cortical

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Dominance of the Proximal Coordinate Frame in Determining the Locations of Hippocampal Place Cell Activity During Navigation

Journal of Neurophysiology ◽

10.1152/jn.00731.2007 ◽

2008 ◽

Vol 99 (1) ◽

pp. 60-76 ◽

Cited By ~ 20

Author(s):

Jennifer J. Siegel ◽

Joshua P. Neunuebel ◽

James J. Knierim

Keyword(s):

Spatial Representation ◽

Reference Frames ◽

Specific Activity ◽

Late Phase ◽

Cell Activity ◽

Coordinate Frame ◽

Spatial Frames Of Reference ◽

Preference Task ◽

Freely Moving ◽

Hippocampal Place Cell

The place-specific activity of hippocampal cells provides downstream structures with information regarding an animal's position within an environment and, perhaps, the location of goals within that environment. In rodents, recent research has suggested that distal cues primarily set the orientation of the spatial representation, whereas the boundaries of the behavioral apparatus determine the locations of place activity. The current study was designed to address possible biases in some previous research that may have minimized the likelihood of observing place activity bound to distal cues. Hippocampal single-unit activity was recorded from six freely moving rats as they were trained to perform a tone-initiated place-preference task on an open-field platform. To investigate whether place activity was bound to the room- or platform-based coordinate frame (or both), the platform was translated within the room at an “early” and at a “late” phase of task acquisition (Shift 1 and Shift 2). At both time points, CA1 and CA3 place cells demonstrated room-associated and/or platform-associated activity, or remapped in response to the platform shift. Shift 1 revealed place activity that reflected an interaction between a dominant platform-based (proximal) coordinate frame and a weaker room-based (distal) frame because many CA1 and CA3 place fields shifted to a location intermediate to the two reference frames. Shift 2 resulted in place activity that became more strongly bound to either the platform- or room-based coordinate frame, suggesting the emergence of two independent spatial frames of reference (with many more cells participating in platform-based than in room-based representations).

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Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats

Neuroscience ◽

10.1016/s0306-4522(02)00700-5 ◽

2003 ◽

Vol 117 (4) ◽

pp. 1025-1035 ◽

Cited By ~ 47

Author(s):

T Kobayashi ◽

A.H Tran ◽

H Nishijo ◽

T Ono ◽

G Matsumoto

Keyword(s):

Cell Activity ◽

Place Cell ◽

Hippocampal Place Cell

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Hippocampal place cells use vector computations to navigate

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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Efficient neural decoding of self-location with a deep recurrent network

10.1101/242867 ◽

2018 ◽

Cited By ~ 1

Author(s):

Ardi Tampuu ◽

Tambet Matiisen ◽

H. Freyja Ólafsdóttir ◽

Caswell Barry ◽

Raul Vicente

Keyword(s):

Hippocampal Neurons ◽

Cell Activity ◽

Recurrent Network ◽

Brain Network ◽

Place Cells ◽

Neuronal Firing ◽

Temporal Context ◽

Central Component ◽

Neural Decoding ◽

Freely Moving

AbstractPlace cells in the mammalian hippocampus signal self-location with sparse spatially stable firing fields. Based on observation of place cell activity it is possible to accurately decode an animal’s location. The precision of this decoding sets a lower bound for the amount of information that the hippocampal population conveys about the location of the animal. In this work we use a novel recurrent neural network (RNN) decoder to infer the location of freely moving rats from single unit hippocampal recordings. RNNs are biologically plausible models of neural circuits that learn to incorporate relevant temporal context without the need to make complicated assumptions about the use of prior information to predict the current state. When decoding animal position from spike counts in 1D and 2D-environments, we show that the RNN consistently outperforms a standard Bayesian model with flat priors. In addition, we also conducted a set of sensitivity analysis on the RNN decoder to determine which neurons and sections of firing fields were the most influential. We found that the application of RNNs to neural data allowed flexible integration of temporal context, yielding improved accuracy relative to a commonly used Bayesian approach and opens new avenues for exploration of the neural code.Author summaryBeing able to accurately self-localize is critical for most motile organisms. In mammals, place cells in the hippocampus appear to be a central component of the brain network responsible for this ability. In this work we recorded the activity of a population of hippocampal neurons from freely moving rodents and carried out neural decoding to determine the animals’ locations. We found that a machine learning approach using recurrent neural networks (RNNs) allowed us to predict the rodents’ true positions more accurately than a standard Bayesian method with flat priors. The RNNs are able to take into account past neural activity without making assumptions about the statistics of neuronal firing. Further, by analyzing the representations learned by the network we were able to determine which neurons, and which aspects of their activity, contributed most strongly to the accurate decoding.

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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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