Dendritic spine heterogeneity and calcium dynamics in basolateral amygdala principal neurons

Glutamatergic synapses on pyramidal neurons are formed on dendritic spines where glutamate activates ionotropic receptors, and calcium influx via N-methyl-d-aspartate receptors leads to a localized rise in spine calcium that is critical for the induction of synaptic plasticity. In the basolateral amygdala, activation of metabotropic receptors is also required for synaptic plasticity and amygdala-dependent learning. Here, using acute brain slices from rats, we show that, in basolateral amygdala principal neurons, high-frequency synaptic stimulation activates metabotropic glutamate receptors and raises spine calcium by releasing calcium from inositol trisphosphate-sensitive calcium stores. This spine calcium release is unevenly distributed, being present in proximal spines, but largely absent in more distal spines. Activation of metabotropic receptors also generated calcium waves that differentially invaded spines as they propagated toward the soma. Dendritic wave invasion was dependent on diffusional coupling between the spine and parent dendrite which was determined by spine neck length, with waves preferentially invading spines with short necks. Spine calcium is a critical trigger for the induction of synaptic plasticity, and our findings suggest that calcium release from inositol trisphosphate-sensitive calcium stores may modulate homosynaptic plasticity through store-release in the spine head, and heterosynaptic plasticity of unstimulated inputs via dendritic calcium wave invasion of the spine head.