Abstract
The basolateral nucleus of the amygdala (BL) is thought to support numerous emotional behaviors through specific microcircuits. These are often thought to be comprised of feedforward networks of principal cells and interneurons. Neither well-understood nor often considered are recurrent and feedback connections, which likely engender oscillatory dynamics within BL. Indeed, oscillations in the gamma frequency range (40-100 Hz) are known to occur in the BL, and yet their origin and effect on local circuits remains unknown. To address this, we constructed a biophysically and anatomically detailed model of the rat BL and its local field potential based on the physiological and anatomical literature, along with in vivo and in vitro data we collected on the activities of neurons within the rat BL. Remarkably, the model produced intermittent gamma oscillations (∼50-70 Hz) whose properties matched those recorded in vivo, including their entrainment of spiking. BL gamma-band oscillations were generated by the intrinsic circuitry, depending upon reciprocal interactions between principal cells and fast-spiking interneurons, while connections within these cell types affected the rhythm’s frequency. The model allowed us to conduct experimentally impossible tests to characterize the synaptic and spatial properties of gamma. The entrainment of individual neurons to gamma depended on the number of afferent connections they received, and gamma bursts were spatially restricted in the BL. Importantly, the gamma rhythm synchronized principal cells and mediated competition between ensembles. Together, these results indicate that the recurrent connectivity of BL expands its computational and communication repertoire.
Significant Statement Using in vitro and in vivo data we develop the first large-scale biophysically and anatomically realistic model of the basolateral amygdala nucleus (BL), which reproduces the dynamics of the in vivo local field potential (LFP). Significantly, it predicts that BL intrinsically generates the transient gamma oscillations observed in vivo. The model permitted exploration of the poorly understood synaptic mechanisms underlying gamma genesis in BL, and the model's ability to compute LFPs at arbitrary numbers of recording sites provided insights into the characteristics of the spatial properties of gamma bursts. Furthermore, we show how gamma synchronizes principal cells to overcome their low firing rates while simultaneously promoting competition, potentially impacting their afferent selectivity and efferent drive, and thus emotional behavior.
Footnotes
Conflict of Interest:
The authors declare they have no conflicts of interest associated with the work contained in this manuscript.
Funding: HHS | National Institutes of Health (NIH), MH087755; HHS | National Institutes of Health (NIH), MH109122.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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