Dopamine D2 receptors are organized in bands in normal human temporal cortex

Abstract

Previous studies have documented a highly compartmentalized and laminar organization of dopamine D2 receptors in human hippocampus, entorhinal and perirhinal cortices. These areas receive input from regions of polysensory association cortices of the superior and inferior temporal sulci that evidence functional modules identified by other techniques. We examined the isocortical regions of temporal lobe for an equally well-differentiated pattern of D2 receptor expression as observed in their paleocortical temporal lobe targets. Using quantitative autoradiography we identified an organization of three-dimensional bands of high concentrations of dopamine D2 receptors throughout the rostral-caudal extent of the normal human temporal cortex. In the coronal plane, these D2 receptor-enriched bands had a columnar appearance with the concentration of D2 receptors almost two-fold higher within the bands than in the immediately adjacent cortex. These D2 receptor-enriched bands had a distinct laminar appearance with a paucity of [ 125I]epidepride binding to D2 receptors over the granule cell layer and higher concentrations of D2 receptors in laminae III and V than in the immediately adjacent cortex. They had a consistent width (mean width of 2.83±0.62 mm) in the coronal plane, but had their long axes in the rostrocaudal plane (some were at least 2500 μm in length). Hence, they exist as three-dimensional D2 receptor-enriched and receptor-poor modules with their long axes in the rostrocaudal plane. Tyrosine hydroxylase-immunoreactive fibers were observed to cross orthogonally to the long axes of the D2 receptor enriched bands. Other monoamine receptors (β-adrenergic, 5-hydroxytryptamine 2), and markers for myelin (anti-myelin basic protein immunohistochemistry), glia (5′-nucleotidase), and energy metabolism (cytochrome oxidase) showed a laminar organization but failed to demarcate the D2 receptor-enriched bands. The majority of these D2 receptor-enriched bands were observed in the lateral and inferior aspects of the superior temporal gyrus, less frequently on the lateral surface of the inferior temporal gyrus and the parahippocampal cortices (Brodmann's area 22, 42 and 20, 21, 37). They were absent from primary auditory cortex (Brodmann's 41). The present study is the first known observation of a modular organization of synaptic elements, identified by D2 receptors, in non-primary sensory cortices of any species. The dopamine D2 receptor-enriched bands were found in regions previously identified as having functional modules that underlie feature extraction. Hence, D2 receptor-enriched and receptor-poor modules may provide a mechanism for functional regulation of compartments within these regions by dopamine.