Parvalbumin-immunoreactive axon terminals in macaque monkey and human prefrontal cortex: Laminar, regional, and target specificity of type I and type II synapses

Abstract

In sensory regions of primate neocortex, the calcium-binding protein parvalbumin (PV) is present in axon terminals that form both Gray's type I (asymmetric) and type II (symmetric) synapses. Those terminals forming type I synapses appear to arise from relay nuclei in the thalamus, whereas those forming type II synapses derive from cortical local circuit neurons. However, whether PV is present in both of these two types of terminals in the association regions of the primate prefrontal cortex (PFC) is not known. In the present study, PV-immunoreactive (IR) axon terminals in the superficial layers (layers 2-3a) of monkey PFC area 9 were found to form exclusively type II synapses onto the dendritic spines (44%), shafts (39%), or somata/axon initial segments (17%) of pyramidal neurons. In contrast, in the middle layers (layers 3b-4), 52% of the PV-IR axon terminals formed type I synapses, and 79% of these terminals contacted dendritic spines. However, in the adjacent area 46, only 12% of the PV-IR terminals in the middle layers formed type I synapses. In addition, the PV-IR axon terminals forming type I synapses were 50% larger than those terminals forming type II synapses. Similar to the macaque monkey, in area 9 of the human PFC, PV-IR axon terminals forming type I synapses onto dendritic spines were found in the middle layers. These findings indicate that PV-IR axon terminals in macaque monkey and human PFC are likely to have both intrinsic and extrinsic sources. In addition, the laminar, regional, and target specificity of the labeled terminals forming type I synapses suggests that they arise from PV-IR neurons in the mediodorsal thalamic nucleus.