Khemka, S; Barnes, G; Dolan, RJ; Bach, DR; (2017) Dissecting the function of hippocampal oscillations in a human anxiety model. Journal of Neuroscience , 37 (29) pp. 6869-6876. 10.1523/JNEUROSCI.1834-16.2017.

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Abstract

Neural oscillations in hippocampus and medial prefrontal cortex (mPFC) are a hallmark of rodent anxiety models that build on conflict between approach and avoidance. Yet, the function of these oscillations, and their expression in humans, remain elusive. Here, we used magnetoencephalography (MEG) to investigate neural oscillations in a task that simulated approach-avoidance conflict, wherein 23 male and female human participants collected monetary tokens under a threat of virtual predation. Probability of threat was learned beforehand by direct experience. Magnitude of threat corresponded to a possible monetary loss, which was on each trial signalled as a quantity. We focused our analyses on an a priori defined region-of-interest, bilateral hippocampus. Oscillatory power under conflict was linearly predicted by threat probability in a location consistent with right mid-hippocampus. This pattern was specific to hippocampus, most pronounced in gamma band, and not explained by spatial movement or anxiety-like behaviour. Gamma power was modulated by slower theta rhythms, and this theta modulation increased with threat probability. Furthermore, theta oscillations in the same location showed greater synchrony with medial prefrontal cortex theta with increased threat probability. Strikingly, these findings were not seen in relation to an increase in threat magnitude, which was explicitly signalled as a quantity and induced similar behavioural responses as learned threat probability. Thus, our findings suggest that the expression of hippocampal and mPFC oscillatory activity in the context of anxiety is specifically linked to threat memory. These findings resonate with neurocomputational accounts of the role played by hippocampal oscillations in memory.SIGNIFICANCE STATEMENTWe employ a biologically relevant approach-avoidance conflict test in humans whilst recording neural oscillations with magnetoencephalography, in order to investigate the expression and function of hippocampal oscillations in human anxiety. Extending non-human studies, we can assign a possible function to hippocampal oscillations in this task, namely threat memory communication. This blends into recent attempts to elucidate the role of brain synchronisation in defensive responses to threat.

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