Dissociation between Dorsal and Ventral Hippocampal Theta Oscillations during Decision-Making

Schmidt, Brandy; Hinman, James R.; Jacobson, Tara K.; Szkudlarek, Emily; Argraves, Melissa; Escabı́, Monty A.; Markus, Etan J.

doi:10.1523/jneurosci.2915-12.2013

Cited by 57 publications

(56 citation statements)

References 65 publications

(27 reference statements)

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“…Although theta oscillations in the vHPC, mPFC, and AMY have been shown to occur less frequently than in the dHPC (Adhikari et al, 2010; Royer et al, 2010; Lesting et al, 2011) this may depend on behavioral task or status. Our observations fit with previous studies showing the emergence of robust theta activity in these areas during exploration (Royer et al, 2010; Patel et al, 2012), decision-making (Schmidt et al, 2013), anxiety (Adhikari et al, 2010), and fear (Lesting et al, 2011). Figure 3 shows representative traces of simultaneously recorded LFPs from the mPFC, dHPC, vHPC, and BLA and respective power spectra where theta activity is visible in all brain areas.…”

Section: Resultssupporting

confidence: 92%

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Jacinto

Reis

Dias

et al. 2013

Front. Behav. Neurosci.

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Exposure to a novel environment triggers the response of several brain areas that regulate emotional behaviors. Here, we studied theta oscillations within the hippocampus (HPC)-amygdala (AMY)-medial prefrontal cortex (mPFC) network in exploration of a novel environment and subsequent familiarization through repeated exposures to that same environment; in addition, we assessed how concomitant stress exposure could disrupt this activity and impair both behavioral processes. Local field potentials (LFP) were simultaneously recorded from dorsal and ventral hippocampus (dHPC and vHPC, respectively), basolateral amygdala (BLA) and mPFC in freely behaving rats while they were exposed to a novel environment, then repeatedly re-exposed over the course of 3 weeks to that same environment and, finally, on re-exposure to a novel unfamiliar environment. A longitudinal analysis of theta activity within this circuit revealed a reduction of vHPC and BLA theta power and vHPC-BLA theta coherence through familiarization which was correlated with a return to normal exploratory behavior in control rats. In contrast, a persistent over-activation of the same brain regions was observed in stressed rats that displayed impairments in novel exploration and familiarization processes. Importantly, we show that stress also affected intra-hippocampal synchrony and heightened the coherence between vHPC and BLA. In summary, we demonstrate that modulatory theta activity in the aforementioned circuit, namely in the vHPC and BLA, is correlated with the expression of anxiety in novelty-induced exploration and familiarization in both normal and pathological conditions.

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Section: Resultssupporting

confidence: 92%

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Jacinto

Reis

Dias

et al. 2013

Front. Behav. Neurosci.

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“…Our results add to others (Montgomery et al, ; Schmidt et al, ) in providing evidence that theta oscillations are related to the computations occurring in the hippocampus during spatial DM. By applying multiple regression analysis to hippocampal LFPs recorded from rats performing a modified T‐maze task (an eight‐shaped maze), Montgomery et al () have previously shown that maze region (e.g., decision arm vs. return arm) better accounts for variations in theta power than locomotion speed.…”

Section: Discussionsupporting

confidence: 86%

“…During waking states, though, behavioral variables have been major confound factors when trying to link theta activity to cognitive function. Although the previous studies have reported that decision points in spatial maze tasks are associated with increases in hippocampal theta power (DeCoteau et al, ; Johnson and Redish, ; Tort et al, ; Montgomery et al, ; Schmidt et al, ), as well as greater theta coherence between the hippocampus and the other brain regions (Jones and Wilson, ; DeCoteau et al, ; Tort et al, ; Benchenane et al, ; Womelsdorf et al, ), in these tasks animals usually traverse at high speeds the arm in which DM is assumed to occur, making it difficult to dissociate behavioral from cognitive influences.…”

Section: Discussionmentioning

confidence: 99%

Increase in hippocampal theta oscillations during spatial decision making

et al. 2014

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The processing of spatial and mnemonic information is believed to depend on hippocampal theta oscillations (5–12 Hz). However, in rats both the power and the frequency of the theta rhythm are modulated by locomotor activity, which is a major confounding factor when estimating its cognitive correlates. Previous studies have suggested that hippocampal theta oscillations support decision-making processes. In this study, we investigated to what extent spatial decision making modulates hippocampal theta oscillations when controlling for variations in locomotion speed. We recorded local field potentials from the CA1 region of rats while animals had to choose one arm to enter for reward (goal) in a four-arm radial maze. We observed prominent theta oscillations during the decision-making period of the task, which occurred in the center of the maze before animals deliberately ran through an arm toward goal location. In speed-controlled analyses, theta power and frequency were higher during the decision period when compared to either an intertrial delay period (also at the maze center), or to the period of running toward goal location. In addition, theta activity was higher during decision periods preceding correct choices than during decision periods preceding incorrect choices. Altogether, our data support a cognitive function for the hippocampal theta rhythm in spatial decision making.

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“…This assumption is supported by the finding that coherence between the dorsal and ventral subregions increase when the rat is confronted with a spatial working memory task (Schmidt et al, 2013). It would be interesting to determine the degree to which dorsal and ventral hippocampal subregions are interdependent during task acquisition.…”

Section: Memory Impairments As a Results Of Muscimol Infusion Have Beenmentioning

confidence: 93%

Interdependence between dorsal and ventral hippocampus during spatial navigation

et al. 2019

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Introduction The hippocampus is linked to the formation and retrieval of episodic memories and spatial navigation. In rats, it is an elongated structure divided into dorsal (septal) and ventral (temporal) regions paralleling the respective division in the posterior and anterior hippocampus in humans. The dorsal hippocampus has been suggested to be more important for spatial processing and the ventral to processing anxiety‐based behaviors. Far less is known regarding the degree to which these different regions interact during information processing. The anatomical connectivity suggests a flow of information between the dorsal and ventral regions; conversely, there are also commissural connections to the contralateral hippocampus. The current study examined the extent to which information from the dorsal hippocampus interacts with processing in the ipsilateral and contralateral ventral hippocampus following the acquisition of a spatial task. Methods Rats were well‐trained on a spatial reference version of the water maze, followed by muscimol inactivation of different hippocampal subregions in a within‐animal repeated design. Various combinations of bilateral, ipsilateral, and contralateral infusions were used. Results Combined dorsal and ventral inactivation produced a severe impairment in spatial performance. Inactivation of only the dorsal or ventral regions resulted in intermediate impairment with performance levels falling between controls and combined inactivation. Performance was impaired during contralateral inactivation and was almost equivalent to bilateral dorsal and ventral hippocampus inactivation, while ipsilateral inactivation resulted in little impairment. Conclusions Taken together, results indicate that for spatial processing, the hippocampus functions as a single integrated structure along the longitudinal axis.

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Dissociation between Dorsal and Ventral Hippocampal Theta Oscillations during Decision-Making

Cited by 57 publications

References 65 publications

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Increase in hippocampal theta oscillations during spatial decision making

Interdependence between dorsal and ventral hippocampus during spatial navigation

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