scholarly journals Place cell firing cannot support navigation without intact septal circuits

2018 ◽  
Author(s):  
Kevin A. Bolding ◽  
Janina Ferbinteanu ◽  
Steven E. Fox ◽  
Robert U. Muller

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.

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Daniel Christopher Haggerty ◽  
Daoyun Ji

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.


2017 ◽  
Author(s):  
Panagiota Theodoni ◽  
Bernat Rovira ◽  
Yingxue Wang ◽  
Alex Roxin

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.


2005 ◽  
Vol 565 (2) ◽  
pp. 579-591 ◽  
Author(s):  
Franco A. Taverna ◽  
John Georgiou ◽  
Robert J. McDonald ◽  
Nancy S. Hong ◽  
Alexander Kraev ◽  
...  

Neuroscience ◽  
2003 ◽  
Vol 117 (4) ◽  
pp. 1025-1035 ◽  
Author(s):  
T Kobayashi ◽  
A.H Tran ◽  
H Nishijo ◽  
T Ono ◽  
G Matsumoto

2021 ◽  
Author(s):  
Jake Ormond ◽  
John O'Keefe

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.


2019 ◽  
Author(s):  
Kathryn McClain ◽  
David Tingley ◽  
David Heeger ◽  
György Buzsáki

AbstractSpiking activity of place cells in the hippocampus encodes the animal’s position as it moves through an environment. Within a cell’s place field, both the firing rate and the phase of spiking in the local theta oscillation contain spatial information. We propose a position-theta-phase (PTP) model that captures the simultaneous expression of the firing-rate code and theta-phase code in place cell spiking. This model parametrically characterizes place fields to compare across cells, time and condition, generates realistic place cell simulation data, and conceptualizes a framework for principled hypothesis testing to identify additional features of place cell activity. We use the PTP model to assess the effect of running speed in place cell data recorded from rats running on linear tracks. For the majority of place fields we do not find evidence for speed modulation of the firing rate. For a small subset of place fields, we find firing rates significantly increase or decrease with speed. We use the PTP model to compare candidate mechanisms of speed modulation in significantly modulated fields, and determine that speed acts as a gain control on the magnitude of firing rate. Our model provides a tool that connects rigorous analysis with a computational framework for understanding place cell activity.SignificanceThe hippocampus is heavily studied in the context of spatial navigation, and the format of spatial information in hippocampus is multifaceted and complex. Furthermore, the hippocampus is also thought to contain information about other important aspects of behavior such as running speed, though there is not agreement on the nature and magnitude of their effect. To understand how all of these variables are simultaneously represented and used to guide behavior, a theoretical framework is needed that can be directly applied to the data we record. We present a model that captures well-established spatial-encoding features of hippocampal activity and provides the opportunity to identify and incorporate novel features for our collective understanding.


Cell Reports ◽  
2018 ◽  
Vol 23 (1) ◽  
pp. 32-38 ◽  
Author(s):  
Maria Diamantaki ◽  
Stefano Coletta ◽  
Khaled Nasr ◽  
Roxana Zeraati ◽  
Sophie Laturnus ◽  
...  

1995 ◽  
Vol 74 (1) ◽  
pp. 322-333 ◽  
Author(s):  
B. H. Bland ◽  
J. Konopacki ◽  
I. J. Kirk ◽  
S. D. Oddie ◽  
C. T. Dickson

1. Single-unit discharge patterns of cells in specific nuclei of the caudal diencephalon were characterized in relation to simultaneously recorded field activity from the stratum moleculare of the dentate gyrus according to the criteria that have been used previously to classify cells in the hippocampal formation (including entorhinal cortex), medial septum, and cingulate cortex. Theta (theta)-related cells were classified as 1) tonic theta-ON, if they discharged nonrhythmically and increased their discharge rates during hippocampal theta relative to large, irregular hippocampal field activity (LIA); 2) tonic theta-OFF, if they discharged nonrhythmically and decreased their discharge rates during theta relative to LIA; or 3) phasic theta-ON, if they discharged rhythmically and in phase with ongoing theta, but nonrhythmically during LIA. Cells not meeting any of the above criteria were classified as nonrelated. 2. Recordings were obtained in a total of 127 cells from the caudal diencephalon. Recordings were made in 54 cells from the posterior hypothalamic nucleus (PH), 16 from the supramammillary nucleus (SuM), 20 from the PH/SuM border, and 23 from the medial mammillary nucleus (MM). Recordings were also made from nine cells from the central medial nucleus of the thalamus (CM) and five from the dorsomedial hypothalamic nucleus (DMH). 3. Of the 54 PH cells, 43 (80%) were classified as tonic theta-ON and 11 (20%) as nonrelated. Tonic theta-ON cells in the PH discharged at significantly higher rates during theta, either occurring spontaneously (9.6 +/- 1.7 Hz, mean +/- SE) or elicited with a tail pinch (TP theta; 10.6 +/- 1.9 Hz), than during LIA (3.6 +/- 1.4 Hz). Of the nine CM cells, seven (78%) were tonic theta-ON and two (22%) were nonrelated. Tonic theta-ON cells discharged at significantly higher rates during theta (17.5 +/- 7.8 Hz) or TP theta (18.0 +/- 7.1 Hz) than during LIA (7.3 +/- 4.8 Hz). All DMH cells were nonrelated. 4. Of the 20 PH/SuM border cells, 15 (75%) were classified as tonic theta-OFF and discharged at significantly higher rates during LIA (5.3 +/- 1.5 Hz) than during theta (0.8 +/- 0.4 Hz) or TP theta (0.4 +/- 0.3 Hz). Five (25%) cells in the PH/SuM border were nonrelated. 5. All of the 16 cells (100%) recorded from the body of the SuM were phasic theta-ON. The discharge rates of these cells did not change significantly across hippocampal field states (LIA = 8.3 +/- 1.6; theta = 7.3 +/- 1.6; TP theta = 8.6 +/- 1.7 Hz).(ABSTRACT TRUNCATED AT 400 WORDS)


2011 ◽  
Vol 106 (5) ◽  
pp. 2749-2763 ◽  
Author(s):  
Hao Zhang ◽  
Shih-Chieh Lin ◽  
Miguel A. L. Nicolelis

The medial septum-vertical limb of the diagonal band of Broca (MSvDB) is important for normal hippocampal functions and theta oscillations. Although many previous studies have focused on understanding how MSVDB neurons fire rhythmic bursts to pace hippocampal theta oscillations, a significant portion of MSVDB neurons are slow-firing and thus do not pace theta oscillations. The function of these MSVDB neurons, especially their role in modulating hippocampal activity, remains unknown. We recorded MSVDB neuronal ensembles in behaving rats, and identified a distinct physiologically homogeneous subpopulation of slow-firing neurons (overall firing <4 Hz) that shared three features: 1) much higher firing rate during rapid eye movement sleep than during slow-wave (SW) sleep; 2) temporary activation associated with transient arousals during SW sleep; 3) brief responses (latency 15∼30 ms) to auditory stimuli. Analysis of the fine temporal relationship of their spiking and theta oscillations showed that unlike the theta-pacing neurons, the firing of these “pro-arousal” neurons follows theta oscillations. However, their activity precedes short-term increases in hippocampal oscillation power in the theta and gamma range lasting for a few seconds. Together, these results suggest that these pro-arousal slow-firing MSvDB neurons may function collectively to promote hippocampal activation.


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