Abstract
The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (∼3-6 Hz), high theta (∼6-12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV, SOM, and VIP) in the BLA can be critically involved in producing the rhythms; these rhythms promote the formation of a dedicated fear circuit shaped through spike-timing-dependent plasticity. Each class of interneurons is necessary for the plasticity. We find that the low theta rhythm is a biomarker of successful fear conditioning. The model makes use of interneurons commonly found in the cortex and, hence, may apply to a wide variety of associative learning situations.
Significance Our paper accounts for the experimental evidence showing that amygdalar rhythms exist, suggests network origins for these rhythms, and points to their central role in the mechanisms of plasticity involved in associative learning. It is one of the few papers to address high-order cognition with biophysically detailed models, which are sometimes thought to be too detailed to be adequately constrained. Our paper provides a template for how to use information about brain rhythms to constrain biophysical models. It shows in detail, for the first time, how multiple interneurons help to provide time scales necessary for some kinds of spike-timing-dependent plasticity (STDP). It spells out the conditions under which such interactions between interneurons are needed for STDP and why. Finally, our work helps to provide a framework by which some of the discrepancies in the fear learning literature might be reevaluated. In particular, we discuss issues about Hebbian plasticity in fear learning; we show in the context of our model how neuromodulation might resolve some of those issues. The model addresses issues more general than that of fear learning since it is based on interactions of interneurons that are prominent in the cortex, as well as the amygdala.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
Several changes were made throughout the paper, especially in the Introduction and Discussion.
