Abstract
The basolateral complex of the amygdala (BLA) is a critical component of the neural circuit regulating fear learning. During fear learning and recall, the amygdala and other brain regions, including the hippocampus and prefrontal cortex, exhibit phase-locked oscillations in the high delta/low theta frequency band (∼2–6 Hz) that have been shown to contribute to the learning process. Network oscillations are commonly generated by inhibitory synaptic input that coordinates action potentials in groups of neurons. In the rat BLA, principal neurons spontaneously receive synchronized, inhibitory input in the form of compound, rhythmic, inhibitory postsynaptic potentials (IPSPs), likely originating from burst-firing parvalbumin interneurons. Here we investigated the role of compound IPSPs in the rat and rhesus macaque BLA in regulating action potential synchrony and spike-timing precision. Furthermore, because principal neurons exhibit intrinsic oscillatory properties and resonance between 4 and 5 Hz, in the same frequency band observed during fear, we investigated whether compound IPSPs and intrinsic oscillations interact to promote rhythmic activity in the BLA at this frequency. Using whole-cell patch clamp in brain slices, we demonstrate that compound IPSPs, which occur spontaneously and are synchronized across principal neurons in both the rat and primate BLA, significantly improve spike-timing precision in BLA principal neurons for a window of ∼300 ms following each IPSP. We also show that compound IPSPs coordinate the firing of pairs of BLA principal neurons, and significantly improve spike synchrony for a window of ∼130 ms. Compound IPSPs enhance a 5 Hz calcium-dependent membrane potential oscillation (MPO) in these neurons, likely contributing to the improvement in spike-timing precision and synchronization of spiking. Activation of the cAMP-PKA signaling cascade enhanced the MPO, and inhibition of this cascade blocked the MPO. We discuss these results in the context of spike-timing dependent plasticity and modulation by neurotransmitters important for fear learning, such as dopamine.
Highlights
The basolateral complex of the amygdala (BLA) is a critical part of the neural circuit regulating fear learning [1,2,3,4,5], and recent evidence suggests that oscillatory activity of neurons in this region plays a key role in regulating affect in awake, behaving animals
We have shown previously that approximately 80% of principal neurons in slice preparations of the rat BLA receive spontaneous, compound inhibitory postsynaptic potentials (IPSPs) that occur rhythmically at frequencies ranging from 0.5–2 Hz, with a mean of 1.2 Hz, in control ACSF [18]
We demonstrate that spontaneous, compound IPSPs function to increase spike-timing precision both within and across BLA principal neurons
Summary
The basolateral complex of the amygdala (BLA) is a critical part of the neural circuit regulating fear learning [1,2,3,4,5], and recent evidence suggests that oscillatory activity of neurons in this region plays a key role in regulating affect in awake, behaving animals (for review, see [6]). Despite the importance of these low frequency oscillations to amygdala function and emotional learning, the mechanisms by which the BLA circuit generates rhythmic activity are largely unknown. BLA principal neurons exhibit compound, rhythmic, inhibitory postsynaptic potentials (IPSPs) that occur at a baseline frequency of 0.5–4 Hz that is sensitive to modulation by dopamine and serotonin [18,19,20]. These rhythmic IPSPs are driven by action potentials in local, burst-firing interneurons, which we have previously shown to express parvalbumin (PV+) [21]. We and others have shown that, in paired recordings of rat BLA principal neurons, spontaneous IPSPs are highly synchronized [26,27], suggesting that the output of PV+ interneurons may coordinate the activity of large numbers of principal neurons
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