Pyramidal cells of the rat basolateral amygdala: Synaptology and innervation by parvalbumin‐immunoreactive interneurons

Abstract

The generation of emotional responses by the basolateral amygdala is largely determined by the balance of excitatory and inhibitory inputs to its principal neurons, the pyramidal cells. The activity of these neurons is tightly controlled by GABAergic interneurons, especially a parvalbumin-positive (PV+) subpopulation that constitutes almost half of all interneurons in the basolateral amygdala. In the present semi-quantitative investigation we studied the incidence of synaptic inputs of PV+ axon terminals onto pyramidal neurons in the rat basolateral nucleus (BLa). Pyramidal cells were identified using calcium/calmodulin-dependent protein kinase II (CaMK) immunoreactivity as a marker. In order to appreciate the relative abundance of PV+ inputs compared to excitatory inputs and other non-PV+ inhibitory inputs, we also analyzed the proportions of asymmetrical (presumed excitatory) synapses and symmetrical (presumed inhibitory) synapses formed by unlabeled axon terminals targeting pyramidal neurons. The results indicate that the perisomatic region of pyramidal cells is innervated almost entirely by symmetrical synapses, whereas the density of asymmetrical synapses increases as one proceeds from thicker proximal dendritic shafts to thinner distal dendritic shafts. The great majority of synapses with dendritic spines are asymmetrical. PV+ axon terminals mainly form symmetrical synapses. These PV+ synapses constitute slightly more than half of the symmetrical synapses formed with each postsynaptic compartment of BLa pyramidal cells. These data indicate that the synaptology of basolateral amygdalar pyramidal cells is remarkably similar to that of cortical pyramidal cells, and that PV+ interneurons provide a robust inhibition of both the perisomatic and distal dendritic domains of these principal neurons. Keywordsimmunocytochemistry; electron microscopy; inhibition, calcium/calmodulin-protein kinase II The basolateral amygdala (ABL), which consists of the lateral, basolateral, and basomedial amygdalar nuclei, is one of the most important brain regions for the generation of emotional behavior and the formation of emotional memories (Aggleton, 1992;Aggleton, 2000;Shinnick-Gallagher et al., 2003). It receives sensory information from the thalamus and cerebral cortex (McDonald, 1998) and produces appropriate emotional responses by activating a variety of subcortical regions including the central amygdalar nucleus, bed nucleus of the stria terminalis, and striatum. The outputs of the ABL arise from pyramidal cells (McDonald, 1992b), which resemble their counterparts in the cerebral cortex. These neurons, which constitute about 85% of the neurons in the ABL, are characterized by a pyramidal or piriform cell body, and spiny dendrites (Hall, 1972;McDonald, 1982McDonald, , 1984 1992a,b;Millhouse and DeOlmos, 1983). Some ABL pyramidal cells have a marked pyramidal morphology, with a clear differentiation of thicker "apical" dendrites from thinner "basal" dendrites, whereas others have a semipyramidal or even stellate appe...

Networks of Parvalbumin-Positive Interneurons in the Basolateral Amygdala

“…Support for this proposed role for DF cells comes from their somatic innervation of principal neurons based on the rapid kinetics of the IPSCs they produce, and their depolarized spike threshold, which would tailor them to regulate excessive principal neuron output. Ultrastructural data showing that ϳ50% of somatic symmetrical synapses express parvalbumin (Muller et al, 2006) is also consistent with this proposal.…”

“…Thus, as with our AC cells, dendritic interneurons possess slower membrane time constants, exhibit spike frequency adaptation, and fire broader action potentials than their somatic counterparts (Beierlein et al, 2003;Jonas et al, 2004;Pouille and Scanziani, 2004). Furthermore, ultrastructural studies have shown that a substantial proportion (20ϳ28%) of PVϩ terminals in the cat (Smith et al, 1998) and rat (Muller et al, 2006) basal amygdala target principal neuron distal dendrites, suggesting a similar anatomical organization of the PVϩ synapses in the three species. It has also been estimated that up to 40% of calbindinexpressing interneurons in the rat basolateral nucleus, the majority of which are likely to also express parvalbumin, target distal principal neuron dendrites (Muller et al, 2003).…”

Heightened Amygdala Long-Term Potentiation in Neurotensin Receptor Type-1 Knockout Mice

“…We suspect that the internal solution was not adequately perfused at the distal site of the thin dendrite, and insufficient exchange of intracellular solution perturbs the shift of the equilibrium potential, leaving it near the original value. This speculation is supported by reports on the presence of GABAergic synapses in distal dendrites in BLA pyramidal neurons (Muller et al, 2006(Muller et al, , 2007.…”

GABAergic Excitation in the Basolateral Amygdala

“…Chandelier synapses have also been described in the amygdala, and these terminals are known to express parvalbumin (Kemppainen and Pitkanen, 2000;McDonald and Betette, 2001;Muller et al, 2006). Because cortical AAC interneurons express parvalbumin (Howard et al, 2005), we tested whether interneurons that provide disynaptic excitation in the amygdala may also make chandelier synapses.…”