scholarly journals Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

2019 ◽  
Author(s):  
Mark C. Zielinski ◽  
Justin D. Shin ◽  
Shantanu P. Jadhav
Keyword(s):  
Prefrontal Cortex ◽  
Spatial Memory ◽  
Spatial Information ◽  
Cell Activity ◽  
Memory Task ◽  
Physiological Mechanism ◽  
Spatial Position ◽  
Theta Oscillations ◽  
Male Rats ◽  
Theta Phase

ABSTRACTInteractions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for memory-guided behavior. Theta oscillations (~8 Hz) underlie a key physiological mechanism for mediating these coordinated interactions, and theta oscillatory coherence and phase-locked spiking in the two regions have been shown to be important for spatial memory. Hippocampal place cell activity associated with theta oscillations encodes spatial position during behavior, and theta-phase associated spiking is known to further mediate a temporal code for space within CA1 place fields. Although prefrontal neurons are prominently phase-locked to hippocampal theta oscillations in spatial memory tasks, whether and how theta oscillations mediate processing of spatial information across these networks remains unclear. Here, we addressed these questions using simultaneous recordings of dorsal CA1 – PFC ensembles and population decoding analyses in male rats performing a continuous spatial working memory task known to require hippocampal-prefrontal interactions. We found that in addition to CA1, population activity in PFC can also encode the animal’s current spatial position on a theta-cycle timescale during memory-guided behavior. Coding of spatial position was coherent for CA1 and PFC ensembles, exhibiting correlated position representations within theta cycles. In addition, incorporating theta-phase information during decoding to account for theta-phase associated spiking resulted in a significant improvement in the accuracy of prefrontal spatial representations, similar to concurrent CA1 representations. These findings indicate a theta-oscillation mediated mechanism of temporal coordination for shared processing and communication of spatial information across the two networks during spatial memory-guided behavior.

scholarly journals Hippocampal theta sequences in REM sleep during spatial learning

2021 ◽  
Author(s):  
Mark C. Zielinski ◽  
Justin D. Shin ◽  
Shantanu P. Jadhav
Keyword(s):  
Rem Sleep ◽  
Cell Activity ◽  
Memory Task ◽  
Neuronal Population ◽  
Phase Shifting ◽  
Theta Oscillations ◽  
Male Rats ◽  
Neuronal Ensembles ◽  
State Dependent ◽  
Hippocampal Theta

ABSTRACTRapid eye movement (REM) sleep is known to play a role in hippocampally-dependent memory, yet the activity and development of hippocampal neuronal ensembles during this state is not well understood. Here we investigated patterning of CA1 place cell activity by theta oscillations, a shared electrophysiological hallmark of both waking behavior and REM sleep, in male rats learning a spatial memory task. We report the existence of REM theta sequences, sequential reactivations of place cells in REM theta that parallel waking theta sequences. REM and wake theta sequences develop rapidly with experience, recapitulating behavioral sequences of compressed space in forward and reverse directions throughout learning. REM sleep exhibited a balance of forward and reverse sequences in contrast to predominantly forward wake theta sequences. Finally, we found that a CA1 neuronal population known to shift preferred theta phases in REM exhibited differential participation in wake and REM theta sequences. In particular, this phase-shifting population showed an increased contribution to REM theta sequence representations after behavioral performance asymptotes and the task is learned, supporting a previously hypothesized role in depotentiation. These findings suggest a role for REM associated theta sequences in state dependent memory functions of the hippocampal circuit, providing evidence that REM sleep is associated with sequence reactivation that can support consolidation of representations necessary for memory guided behavior.

scholarly journals Position-theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate

2019 ◽  
Author(s):  
Kathryn McClain ◽  
David Tingley ◽  
David Heeger ◽  
György Buzsáki
Keyword(s):  
Firing Rate ◽  
Spatial Information ◽  
Cell Activity ◽  
Gain Control ◽  
Place Cell ◽  
Small Subset ◽  
Running Speed ◽  
Speed Modulation ◽  
Place Fields ◽  
Theta Phase

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.

Theta power and theta-gamma coupling support spatial memory retrieval

2019 ◽  
Author(s):  
Umesh Vivekananda ◽  
Daniel Bush ◽  
James A Bisby ◽  
Sallie Baxendale ◽  
Roman Rodionov ◽  
...  
Keyword(s):  
Spatial Memory ◽  
Task Performance ◽  
Memory Function ◽  
Memory Task ◽  
Theta Oscillations ◽  
Theta Power ◽  
Human Epilepsy ◽  
Phase Amplitude ◽  
Hippocampal Theta

AbstractHippocampal theta oscillations have been implicated in spatial memory function in both rodents and humans. What is less clear is how hippocampal theta interacts with higher frequency oscillations during spatial memory function, and how this relates to subsequent behaviour. Here we asked ten human epilepsy patients undergoing intracranial EEG recording to perform a desk-top virtual reality spatial memory task, and found that increased theta power in two discrete bands (‘low’ 2-5Hz and ‘high’ 6-9Hz) during cued retrieval was associated with improved task performance. Similarly, increased coupling between ‘low’ theta phase and gamma amplitude during the same period was associated with improved task performance. These results support a role of theta oscillations and theta-gamma phase-amplitude coupling in human spatial memory function.

scholarly journals Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex

2019 ◽  
Vol 39 (23) ◽  
pp. 4550-4565 ◽  
Author(s):  
Mark C. Zielinski ◽  
Justin D. Shin ◽  
Shantanu P. Jadhav
Keyword(s):  
Prefrontal Cortex ◽  
Spatial Position ◽  
Theta Oscillations

Spatial Memory and Response Strategies in Rats: Age, Sex and Rearing Differences in Performance

1980 ◽  
Vol 32 (3) ◽  
pp. 473-489 ◽  
Author(s):  
Dorothy Einon
Keyword(s):  
Spatial Memory ◽  
Social Isolation ◽  
Social Housing ◽  
Memory Task ◽  
Spatial Abilities ◽  
Male Rats ◽  
Spatial Memory Task ◽  
Response Strategies ◽  
Old Rats ◽  
The Difference

Rats reared in social isolation made more errors on a spatial memory task and made errors earlier in each trial than socially reared rats. The difference in performance only occurred when rats were isolated prior to 50 days of age, and it survived IOO days of subsequent social housing. IOO days of isolation after 50 days of age did not influence performance on the spatial memory task. Subsequent experiments suggest that spatial abilities may not differ between groups but that isolates are slower to learn to make a particular response and to locate a particular arm when spatial and response cues are irrelevant. In contrast to previous experiments, clear response strategies were seen in the present experiments. These were prevalent in the young (54-days-old) rats, were less common at 90 days and had completely disappeared by 180 days. Response strategies were more common in male rats and in socially reared rats.

Dissociations in the Processing of “What” and “Where” Information in Working Memory: An Event-Related Potential Analysis

1996 ◽  
Vol 8 (5) ◽  
pp. 453-473 ◽  
Author(s):  
A. Mecklinger ◽  
N. Müller
Keyword(s):  
Working Memory ◽  
Spatial Memory ◽  
Slow Wave ◽  
Spatial Information ◽  
Test Procedure ◽  
Memory Task ◽  
Event Related Potential ◽  
Study Phase ◽  
Object Memory ◽  
Spatial Memory Task

Based on recent research that suggests that the processing of spatial and object information in the primate brain involves functionally and anatomically different systems, we examined whether the encoding and retention of object and spatial information in working memory are associated with different ERP components. In a study-test procedure subjects were asked to either remember simple geometric objects presented in a 4 by 4 spatial matrix irrespective of their position (object memory task) or to remember spatial positions of the objects irrespective of their forms (spatial memory task). The EEG was recorded from 13 electrodes during the study phase and the test phase. Recognition performance (reaction time and accuracy) was not different for the two memory tasks. PCA analyses suggest that the same four ERP components are evoked in the study phase by both tasks, which could be identified as N100, P200, P300, and slow wave. ERPs started to differ as a function of memory task 225 msec after stimulus onset at the posterior recording sites: An occipital maximal P200 component, lateralized to the right posterior temporal recording site, was observed for the object memory but not for the spatial memory task. Between-tasks differences were also obtained for P300 scalp distribution. Moreover, ERPs evoked by objects that were remembered later were more positive than ERPs to objects that were not remembered, starting at 400 msec postsimulus. The PCA analysis suggest that P300 and a slow wave following P300 at the frontal recordings contribute to these differences. A similar differential effect was not found between positions remembered or not remembered later. Post hoc analyses revealed that the absence of such effects in the spatial memory task could be due to less elaborated mnemonic strategies used in the spatial task compared to the object memory task. In the face of two additional behavioral experiments showing that subjects exclusively encode object features in the object memory task and spatial stimulus features in the spatial memory task, the present data provide evidence that encoding and rehearsal of object and spatial information in working memory are subserved by functionally and anatomically different subsystems.

scholarly journals Functional Metaplasticity of Hippocampal Schaffer Collateral-CA1 Synapses Is Reversed in Chronically Epileptic Rats

2017 ◽  
Vol 2017 ◽  
pp. 1-8 ◽  
Author(s):  
Mirko Rehberg ◽  
Timo Kirschstein ◽  
Xiati Guli ◽  
Steffen Müller ◽  
Marco Rohde ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Spatial Memory ◽  
Spatial Information ◽  
Memory Task ◽  
Long Term Potentiation ◽  
Memory Training ◽  
Control Group ◽  
Training Task ◽  
Schaffer Collateral

Spatial learning and associating spatial information with individual experience are crucial for rodents and higher mammals. Hence, studying the cellular and molecular cascades involved in the key mechanism of information storage in the brain, synaptic plasticity, has led to enormous knowledge in this field. A major open question applies to the interdependence between synaptic plasticity and its behavioral correlates. In this context, it has become clear that behavioral aspects may impact subsequent synaptic plasticity, a phenomenon termed behavioral metaplasticity. Here, we trained control and pilocarpine-treated chronically epileptic rats of two different age groups (adolescent and adult) in a spatial memory task and subsequently tested long-term potentiation (LTP) in vitro at Schaffer collateral—CA1 synapses. As expected, memory acquisition in the behavioral task was significantly impaired both in pilocarpine-treated animals and in adult controls. Accordingly, these groups, without being tested in the behavioral training task, showed reduced CA1-LTP levels compared to untrained young controls. Spatial memory training significantly reduced subsequent CA1-LTP in vitro in the adolescent control group yet enhanced CA1-LTP in the adult pilocarpine-treated group. Such training in the adolescent pilocarpine-treated and adult control groups resulted in intermediate changes. Our study demonstrates age-dependent functional metaplasticity following a spatial memory training task and its reversal under pathological conditions.

scholarly journals Orthogonal representation of task-related information in theta phase-based multiple place fields of single units in the subiculum

2021 ◽  
Author(s):  
Su-Min Lee ◽  
Jae-Min Seol ◽  
Inah Lee
Keyword(s):  
Theta Rhythm ◽  
Memory Task ◽  
Field Size ◽  
Male Rats ◽  
Choice Response ◽  
Neural Firing ◽  
Related Factors ◽  
Related Information ◽  
Phase Precession ◽  
Theta Phase

The subiculum is positioned at a critical juncture at the interface of the hippocampus with the rest of the brain. However, the exact roles of the subiculum in most hippocampal-dependent memory tasks remain largely unknown. One obstacle to make analytical comparisons of neural firing patterns between the subiculum and hippocampal CA1 is the broad firing fields of the subicular cells. Here, we used spiking phases in relation to theta rhythm to parse the broad firing field of a subicular neuron into multiple subfields to find the unique functional contribution of the subiculum while male rats performed a hippocampal-dependent visual scene memory task. Some of the broad firing fields of the subicular neurons were successfully divided into multiple subfields by using the theta-phase precession cycle. The resulting phase-based fields in the subiculum were more similar to those in CA1 in terms of the field size and phase-precession strength. The new method significantly improved the detection of task-relevant information in subicular cells without affecting the information content represented by CA1 cells. Notably, multiple fields of a single subicular neuron, unlike those in the CA1, could carry heterogeneous task-related information such as visual context and choice response. Our findings suggest that the subicular cells integrate multiple task-related factors by using theta rhythm to associate environmental context with action.

scholarly journals In-vivo evidence for proximodistal heterogeneity in hippocampal CA1 and CA3 during non-spatial memory retrieval

2020 ◽  
Author(s):  
Shihpi Ku ◽  
Erika Atucha ◽  
Nico Alavi ◽  
Magdalena Sauvage
Keyword(s):  
Spatial Memory ◽  
Spatial Information ◽  
Memory Task ◽  
Early Gene ◽  
Support Vector ◽  
Study Phase ◽  
Spatial Network ◽  
Ca1 Neurons ◽  
Odor Memory

Recent immediate early gene evidence suggests that proximal CA3 (proxCA3, close to dentate gyrus) and distal CA1 (distCA1, close to subiculum) form a specialized non-spatial hippocampal subnetwork (nakamura et al, JON, 2013; Beer and Vavra, Plos Biology, 2018) while distal CA3 (distCA3) and proximal CA1 (proxCA1) are more specialized in spatial information processing (Flashbeck et al, 2018). However, direct in-vivo evidence for such functional networks are still missing. Here, we used chronically implanted multi-tetrode recording technique to simultaneously record along the proximodistal axis of the two CA-fields while rats performed a high-demanding delayed non-match to odor memory task. In this task, rats smelled 10 (old) odors during the study phase, and after a 20-minute delay memory for the studied odors was tested by exposing rats to the same odors intermixed with 10 new odors. We recorded 193 CA3- and 367 CA1-neurons in 5 animals who could perfom above threshold (75%). Using Support Vector Machine (SVM) we tested whether proxCA3-distCA1 neurons (non-spatial network) can differentiate the old from new odors better than distCA3-proxCA1 neurons (spatial network). We found that activity in the proxCA3-distCA1 network was relevant for the discrimination between old from new odors and similar to behavior; in contrast, the activity of the distCA3-proxCA1 network was not. Further, we found a gradient in the distribution of task-relevant neurons along the transverse axis of CA1 as well as CA3. Overall, we provide clear in vivo electrophysiological evidence that supports the role of proxCA3-distCA1 network in non-spatial memory processing.

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