Multimodal and Site-Specific Plasticity of Amygdala Parvalbumin Interneurons after Fear Learning

Abstract

Summary Stimulus processing in fear conditioning is constrained by parvalbumin-interneurons (PV-INs) through inhibition of principal excitatory neurons. However, the contributions of PV-IN microcircuits to input gating and long-term plasticity in the fear system remain unknown. Here we interrogate synaptic connections between afferent pathways, PV-INs, and principal excitatory neurons in the basolateral amygdala. We find that this region is populated by at least two functionally distinct PV-IN networks based on nucleus location. PV-INs in the lateral (LA), but not the basal (BA), amygdala possess complex dendritic arborizations, receive potent excitatory drive, and mediate feedforward inhibition onto principal neurons. After fear conditioning, PV-INs exhibit nucleus- and target-selective plasticity, resulting in persistent reduction of their excitatory input and inhibitory output in LA but not BA. These data reveal previously overlooked specializations of PV-INs within amygdala subnuclei and indicate specific circuit mechanisms for inhibitory plasticity during the encoding of associative fear memories.

Dopamine in the basal amygdala signals salient somatosensory events during fear learning

“…5) supports the notion that dopamine can contribute to a "teaching" signal for plasticity in the BA (Herry and Johansen, 2014). On the other hand, the LA, which receives many sensory inputs from cortical and thalamic areas (LeDoux et al, 1990;Nabavi et al, 2014;Lucas et al, 2016), was only sparsely innervated by dopamine fibers from the VTA (Fig. 1).…”

Perineuronal nets labeled by monoclonal antibody VC1.1 ensheath interneurons expressing parvalbumin and calbindin in the rat amygdala

“…It is possible that reduced LTP of disynaptic inhibition, which entails glutamatergic inputs to feedforward interneurons, could involve excitatory thalamic inputs onto PV+ interneurons which have had their PNNs degraded since PV+ interneurons in the lateral nucleus receive potent excitatory inputs from the thalamus and mediate feedforward inhibition onto pyramidal cells (Woodson et al, 2000; Lucas et al, 2016). A decrease in the excitability of these PV+ interneurons, which occurs in cortical PV+ neurons with degraded PNNs (see above), might contribute to the reduction in LTP.…”

Closing the gap: long-term presynaptic plasticity in brain function and disease

“…Parvalbumin (PV)-positive interneurons in the LA receive robust excitatory input and mediate powerful FFI onto principal neurons. After fear conditioning, both excitatory inputs –which carry cued auditory information– and inhibitory output of PV interneurons are persistently reduced in a presynaptic manner as indicated by a reduction in paired-pulse ratio [58]. The reduction of GABA release onto LA principal neurons may facilitate subsequent amygdala recruitment by sensory stimuli, thereby contributing to fear learning.…”