Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task.
Ontology highlight
ABSTRACT:
SUBMITTER: Jones MW
PROVIDER: S-EPMC1283536 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Cross-frequency coupling supports the organization of brain rhythms and is present during a range of cognitive functions. However, little is known about whether and how long-range cross-frequency coupling across distant brain regions subserves working memory. Here we report that theta-slow gamma coupling between the hippocampus and medial prefrontal cortex (mPFC) is augmented in a genetic mouse model of cognitive dysfunction. This increased cross-frequency coupling is observed specifically when the mice successfully perform a spatial working memory task. In wild-type mice, increasing task difficulty by introducing a long delay or by optogenetically interfering with encoding, also increases theta-gamma coupling during correct trials. Finally, epochs of high hippocampal theta-prefrontal slow gamma coupling are associated with increased synchronization of neurons within the mPFC. These findings suggest that enhancement of theta-slow gamma coupling reflects a compensatory mechanism to maintain spatial working memory performance in the setting of increased difficulty.
| S-EPMC5736608 | biostudies-literature
Project description:Humans can rapidly and seemingly implicitly learn to predict typical locations of relevant items when those items are encountered in familiar spatial contexts. Two important questions remain, however, concerning this type of learning: (1) which neural structures and mechanisms are involved in acquiring and exploiting such contextual knowledge? (2) Is this type of learning truly implicit and unconscious? We now answer both these questions after closely examining behavior and recording neural activity using MEG while observers (male and female) were acquiring and exploiting statistical regularities. Computational modeling of behavioral data suggested that, after repeated exposures to a spatial context, participants' behavior was marked by an abrupt switch to an exploitation strategy of the learnt regularities. MEG recordings showed that hippocampus and prefrontal cortex (PFC) were involved in the task and furthermore revealed a striking dissociation: only the initial learning phase was associated with hippocampal theta band activity, while the subsequent exploitation phase showed a shift in theta band activity to the PFC. Intriguingly, the behavioral benefit of repeated exposures to certain scenes was inversely related to explicit awareness of such repeats, demonstrating the implicit nature of the expectations acquired. Together, these findings demonstrate that (1a) hippocampus and PFC play complementary roles in the implicit, unconscious learning and exploitation of spatial statistical regularities; (1b) these mechanisms are implemented in the theta frequency band; and (2) contextual knowledge can indeed be acquired unconsciously, and awareness of such knowledge can even interfere with the exploitation thereof.SIGNIFICANCE STATEMENT Human visual perception is determined not just by the light that strikes our eyes, but also strongly by our prior knowledge and expectations. Such expectations, particularly about where to expect certain objects given scene context, might be learned implicitly and unconsciously, although this is hotly debated. Furthermore, it is unknown which brain mechanisms underpin this type of learning. We now show that, indeed, spatial prior expectations can be learned without awareness; in fact, strikingly, awareness seems to hinder the exploitation of the relevant knowledge. Furthermore, we demonstrate that one brain mechanism (hippocampal theta-band activity) is responsible for learning in these settings, whereas another mechanism (prefrontal theta-band activity) is involved in exploiting the learned associations.
| S-EPMC6939492 | biostudies-literature
Project description:Short-term memory enables incorporation of recent experience into subsequent decision-making. This processing recruits both the prefrontal cortex and hippocampus, where neurons encode task cues, rules, and outcomes. However, precisely which information is carried when, and by which neurons, remains unclear. Using population decoding of activity in rat medial prefrontal cortex (mPFC) and dorsal hippocampal CA1, we confirm that mPFC populations lead in maintaining sample information across delays of an operant non-match to sample task, despite individual neurons firing only transiently. During sample encoding, distinct mPFC subpopulations joined distributed CA1-mPFC cell assemblies hallmarked by 4-5 Hz rhythmic modulation; CA1-mPFC assemblies re-emerged during choice episodes but were not 4-5 Hz modulated. Delay-dependent errors arose when attenuated rhythmic assembly activity heralded collapse of sustained mPFC encoding. Our results map component processes of memory-guided decisions onto heterogeneous CA1-mPFC subpopulations and the dynamics of physiologically distinct, distributed cell assemblies.
| S-EPMC10728550 | biostudies-literature
Project description:Previous work has hinted that prospective and retrospective coding modes exist in hippocampus. Prospective coding is believed to reflect memory retrieval processes, whereas retrospective coding is thought to be important for memory encoding. Here, we show in rats that separate prospective and retrospective modes exist in hippocampal subfield CA1 and that slow and fast gamma rhythms differentially coordinate place cells during the two modes. Slow gamma power and phase locking of spikes increased during prospective coding; fast gamma power and phase locking increased during retrospective coding. Additionally, slow gamma spikes occurred earlier in place fields than fast gamma spikes, and cell ensembles retrieved upcoming positions during slow gamma and encoded past positions during fast gamma. These results imply that alternating slow and fast gamma states allow the hippocampus to switch between prospective and retrospective modes, possibly to prevent interference between memory retrieval and encoding.
| S-EPMC4109650 | biostudies-literature
Project description:We compared the dynamics of hippocampal and prefrontal interactions in rats as they used spatial contexts to guide the retrieval of object memories. Functional connectivity analysis indicated a flow of contextual information from the hippocampus to prefrontal cortex upon the rat's entry into the spatial context. Conversely, upon the onset of object sampling, the direction of information flow reversed, consistent with prefrontal control over the retrieval of context-appropriate hippocampal memory representations.
| S-EPMC4961615 | biostudies-literature
Project description:Spatial working memory, the caching of behaviourally relevant spatial cues on a timescale of seconds, is a fundamental constituent of cognition. Although the prefrontal cortex and hippocampus are known to contribute jointly to successful spatial working memory, the anatomical pathway and temporal window for the interaction of these structures critical to spatial working memory has not yet been established. Here we find that direct hippocampal-prefrontal afferents are critical for encoding, but not for maintenance or retrieval, of spatial cues in mice. These cues are represented by the activity of individual prefrontal units in a manner that is dependent on hippocampal input only during the cue-encoding phase of a spatial working memory task. Successful encoding of these cues appears to be mediated by gamma-frequency synchrony between the two structures. These findings indicate a critical role for the direct hippocampal-prefrontal afferent pathway in the continuous updating of task-related spatial information during spatial working memory.
| S-EPMC4505751 | biostudies-literature
Project description:Sevoflurane can induce memory impairment during clinical anesthesia; however, the underlying mechanisms are largely unknown. TASK-3 channels are one of the potential targets of sevoflurane. Accumulating evidence supports a negative role of intracranial theta rhythms (4-12 Hz) in memory formation. Here, we investigated whether TASK-3 channels contribute to sevoflurane-induced memory impairment by regulating hippocampal theta rhythms. In this study, the memory performance of mice was tested by contextual fear conditioning and inhibitory avoidance experiments. The hippocampal local field potentials (LFPs) were recorded from chronically implanted electrodes located in CA3 region. The results showed that sevoflurane concentration-dependently impaired the memory function of mice, as evidenced by the decreased time mice spent on freezing and reduced latencies for mice to enter the shock compartment. Our electrophysiological results revealed that sevoflurane also enhanced the spectral power of hippocampal LFPs (1-30 Hz), particularly in memory-related theta rhythms (4-12 Hz). These effects were mitigated by viral-mediated knockdown of TASK-3 channels in the hippocampal CA3 region. The knockdown of hippocampal TASK-3 channels significantly reduced the enhancing effect of sevoflurane on hippocampal theta rhythms and alleviated sevoflurane-induced memory impairment. Our data indicate that sevoflurane can increase hippocampal theta oscillations and impair memory function via TASK-3 channels.
| S-EPMC8581481 | biostudies-literature
Project description:Hippocampal theta rhythm is believed to play a critical role in learning and memory. In animal models of temporal lobe epilepsy (TLE), there is evidence that alterations of hippocampal theta oscillations are involved in the cognitive impairments observed in this model. However, hippocampal theta frequency and amplitude at both the local field potential (LFP) and single unit level are strongly modulated by running speed, suggesting that the integration of locomotor information into memory processes may also be critical for hippocampal processing. Here, we investigate whether hippocampal speed-theta integration influences spatial memory and whether it could account for the memory deficits observed in TLE rats. LFPs were recorded in both Control (CTR) and TLE rats as they were trained in a spatial alternation task. TLE rats required more training sessions to perform the task at CTR levels. Both theta frequency and power were significantly lower in the TLE group. In addition, speed/theta frequency correlation coefficients and regression slopes varied from session to session and were worse in TLE. Importantly, there was a strong relationship between speed/theta frequency parameters and performance. Our analyses reveal that speed/theta frequency correlation with performance cannot merely be explained by the direct influence of speed on behavior. Therefore, variations in the coordination of theta frequency with speed may participate in learning and memory processes. Impairments of this function could explain at least partially memory deficits in epilepsy.
| S-EPMC5410367 | biostudies-literature
Project description:The striatum and hippocampus are conventionally viewed as complementary learning and memory systems, with the hippocampus specialized for fact-based episodic memory and the striatum for procedural learning and memory. Here we directly tested whether these two systems exhibit independent or coordinated activity patterns during procedural learning. We trained rats on a conditional T-maze task requiring navigational and cue-based associative learning. We recorded local field potential (LFP) activity with tetrodes chronically implanted in the caudoputamen and the CA1 field of the dorsal hippocampus during 6-25 days of training. We show that simultaneously recorded striatal and hippocampal theta rhythms are modulated differently as the rats learned to perform the T-maze task but nevertheless become highly coherent during the choice period of the maze runs in rats that successfully learned the task. Moreover, in the rats that acquired the task, the phase of the striatal-hippocampal theta coherence was modified toward a consistent antiphase relationship, and these changes occurred in proportion to the levels of learning achieved. We suggest that rhythmic oscillations, including theta-band activity, could influence not only neural processing in cortico-basal ganglia circuits but also dynamic interactions between basal ganglia-based and hippocampus-based forebrain circuits during the acquisition and performance of learned behaviors. Experience-dependent changes in coordination of oscillatory activity across brain structures thus may parallel the well known plasticity of spike activity that occurs as a function of experience.
| S-EPMC1838454 | biostudies-literature
Project description:Learning the location of relevant places in the environment is crucial for survival. Such capacity is supported by a distributed network comprising the prefrontal cortex and hippocampus, yet it is not fully understood how these structures cooperate during spatial reference memory formation. Hence, we examined neural activity in the prefrontal-hippocampal circuit in mice during acquisition of spatial reference memory. We found that interregional oscillatory coupling increased with learning, specifically in the slow-gamma frequency (20 to 40 Hz) band during spatial navigation. In addition, mice used both spatial and nonspatial strategies to navigate and solve the task, yet prefrontal neuronal spiking and oscillatory phase coupling were selectively enhanced in the spatial navigation strategy. Lastly, a representation of the behavioral goal emerged in prefrontal spiking patterns exclusively in the spatial navigation strategy. These results suggest that reference memory formation is supported by enhanced cortical connectivity and evolving prefrontal spiking representations of behavioral goals.
| S-EPMC6142212 | biostudies-literature