Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences

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 (PNs) 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 (LFP) 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 PNs and fast-spiking interneurons (FSIs), 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 PNs and mediated competition between ensembles. Together, these results indicate that the recurrent connectivity of BL expands its computational and communication repertoire.

Optogenetic Stimulation of the Basolateral Amygdala Increased Theta-Modulated Gamma Oscillations in the Hippocampus

“…BLA LFPs were characterized by evoked responses of the same width (approximately 9 ms) in the 8, 20, 50, and 50/8 Hz conditions (Figure 3B–F). The initial evoked responses were followed by smaller responses in the fast gamma range (60–120 Hz), which is a prominent frequency band in the amygdala (Amir et al, 2018; Feng et al, 2019). In contrast, CA1 LFPs during stimulation with blue light displayed a more continuous waveform that had a sawtooth shape for 8 and 20 Hz conditions and a sinusoidal shape for 50 Hz stimulation (Figure 3B–D).…”

Noise in Neurons and Synapses Enables Reliable Associative Memory Storage in Local Cortical Circuits

“…6 , second line) and, at critical capacity, the neuron operates in a balanced regime in which inhibitory and excitatory currents are anti-correlated and largely cancel each other out ( Rubin et al, 2017 ). Experimentally, it has been shown that inhibitory postsynaptic currents are larger in magnitude than excitatory ( Atallah and Scanziani, 2009 ; Salkoff et al, 2015 ; Feng et al, 2019 ). Although Equation 14 derived in the N → ∞ limit yield a small positive or zero average postsynaptic input (high-weight regime), associative networks of finite-size loaded with memories to capacity show a trend consistent with the experimental measurements ( Zhang et al, 2019b ).…”

“…(6)] and, at critical capacity, the neuron operates in a balanced regime in which inhibitory and excitatory currents are anti-correlated and largely cancel each other out (Rubin et al, 2017). Experimentally, it has been shown that inhibitory postsynaptic currents are larger in magnitude than excitatory (Atallah and Scanziani, 2009;Salkoff et al, 2015;Feng et al, 2019). Though Eqs.…”

Embracing Complexity in Defensive Networks

“…The BLA also contains reciprocally connected PNs and FSIs, in similar proportions as in cortex (McDonald and Mascagni, 2001;Woodruff and Sah, 2007), and it too exhibits gamma (Bauer et al, 2007;Amir et al, 2018;Stujenske et al, 2014). Indeed, PNs and FSIs of the BLA preferentially spike during gamma oscillations in a manner similar to their cortical counterparts (Amir et al, 2018), and a detailed biophysical model of the BL nucleus generated gamma autonomously, reproducing the properties of gamma recorded in vivo (Feng et al, 2019).…”