Dataset Information

Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations.

ABSTRACT: Detecting environmental change is fundamental for adaptive behavior in an uncertain world. Previous work indicates the hippocampus supports the generation of novelty signals via implementation of a match-mismatch detector that signals when an incoming sensory input violates expectations based on past experience. While existing work has emphasized the particular contribution of the hippocampus, here we ask which other brain structures also contribute to match-mismatch detection. Furthermore, we leverage the fine-grained temporal resolution of magnetoencephalography (MEG) to investigate whether mismatch computations are spectrally confined to the theta range, based on the prominence of this range of oscillations in models of hippocampal function. By recording MEG activity while human subjects perform a task that incorporates conditions of match-mismatch novelty we show that mismatch signals are confined to the theta band and are expressed in both the hippocampus and ventromedial prefrontal cortex (vmPFC). Effective connectivity analyses (dynamic causal modeling) show that the hippocampus and vmPFC work as a functional circuit during mismatch detection. Surprisingly, our results suggest that the vmPFC drives the hippocampus during the generation and processing of mismatch signals. Our findings provide new evidence that the hippocampal-vmPFC circuit is engaged during novelty processing, which has implications for emerging theories regarding the role of vmPFC in memory.

SUBMITTER: Garrido MI

PROVIDER: S-EPMC4594308 | biostudies-literature | 2015 Oct

REPOSITORIES: biostudies-literature

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Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations.

Garrido Marta I MI Barnes Gareth R GR Kumaran Dharshan D Maguire Eleanor A EA Dolan Raymond J RJ

NeuroImage 20150714

Detecting environmental change is fundamental for adaptive behavior in an uncertain world. Previous work indicates the hippocampus supports the generation of novelty signals via implementation of a match-mismatch detector that signals when an incoming sensory input violates expectations based on past experience. While existing work has emphasized the particular contribution of the hippocampus, here we ask which other brain structures also contribute to match-mismatch detection. Furthermore, we l ...[more]

PMID: 26187453

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Project description:Interactions 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.SIGNIFICANCE STATEMENT Theta oscillation- (?8 Hz) mediated interactions between the hippocampus and prefrontal cortex are known to be important for spatial memory. Hippocampal place-cell activity associated with theta oscillations underlies a rate and temporal code for spatial position, but it is not known whether these oscillations mediate simultaneous coding of spatial information in hippocampal-prefrontal networks. Here, we found that population activity in prefrontal cortex encodes animals' current position coherently with hippocampal populations on a theta-cycle timescale. Further we found that theta phase-associated spiking significantly improves prefrontal coding of spatial position, in parallel with hippocampal coding. Our findings establish that theta oscillations mediate a temporal coordination mechanism for coherent coding of spatial position in hippocampal-prefrontal networks during memory-guided behavior.

Dataset Information

Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations.

Publications

Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations.

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