Dataset Information

Hippocampal-Prefrontal Theta Transmission Regulates Avoidance Behavior.

ABSTRACT: Long-range synchronization of neural oscillations correlates with distinct behaviors, yet its causal role remains unproven. In mice, tests of avoidance behavior evoke increases in theta-frequency (?8 Hz) oscillatory synchrony between the ventral hippocampus (vHPC) and medial prefrontal cortex (mPFC). To test the causal role of this synchrony, we dynamically modulated vHPC-mPFC terminal activity using optogenetic stimulation. Oscillatory stimulation at 8 Hz maximally increased avoidance behavior compared to 2, 4, and 20 Hz. Moreover, avoidance behavior was selectively increased when 8-Hz stimulation was delivered in an oscillatory, but not pulsatile, manner. Furthermore, 8-Hz oscillatory stimulation enhanced vHPC-mPFC neurotransmission and entrained neural activity in the vHPC-mPFC network, resulting in increased synchrony between vHPC theta activity and mPFC spiking. These data suggest a privileged role for vHPC-mPFC theta-frequency communication in generating avoidance behavior and provide direct evidence that synchronized oscillations play a role in facilitating neural transmission and behavior.

SUBMITTER: Padilla-Coreano N

PROVIDER: S-EPMC6842114 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Publications

Hippocampal-Prefrontal Theta Transmission Regulates Avoidance Behavior.

Padilla-Coreano Nancy N Canetta Sarah S Mikofsky Rachel M RM Alway Emily E Passecker Johannes J Myroshnychenko Maxym V MV Garcia-Garcia Alvaro L AL Warren Richard R Teboul Eric E Blackman Dakota R DR Morton Mitchell P MP Hupalo Sofiya S Tye Kay M KM Kellendonk Christoph C Kupferschmidt David A DA Gordon Joshua A JA

Neuron 20190911 3

Long-range synchronization of neural oscillations correlates with distinct behaviors, yet its causal role remains unproven. In mice, tests of avoidance behavior evoke increases in theta-frequency (∼8 Hz) oscillatory synchrony between the ventral hippocampus (vHPC) and medial prefrontal cortex (mPFC). To test the causal role of this synchrony, we dynamically modulated vHPC-mPFC terminal activity using optogenetic stimulation. Oscillatory stimulation at 8 Hz maximally increased avoidance behavior ...[more]

PMID: 31521441

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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.

Dataset Information

Hippocampal-Prefrontal Theta Transmission Regulates Avoidance Behavior.

Publications

Hippocampal-Prefrontal Theta Transmission Regulates Avoidance Behavior.

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