Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: A radioautographic study

Abstract

The regional density and laminar distribution of dopamine (DA) and serotonin (5-HT) afferents were investigated in the cerebral cortex of cynomolgus monkeys using a radioautographic technique that is based on the high affinity uptake capacity of these aminergic neurons. Large vibratome sections, 50 micron thick, were incubated with [3H] DA (0.2 microM) and desipramine (5 microM) or with unlabeled norepinephrine (5 microM) and [3H] 5-HT (0.6 microM), which allowed for the specific labeling of the DA and 5-HT innervations, respectively. After fixation, these sections were dried, defatted, and radioautographed by dipping. Semiquantitative data on the DA innervation also were provided by counting [3H] DA-labeled axonal varicosities in radioautographs from 4-micron-thick sections of the slices obtained after epon embedding. The DA innervation was widespread and differed in density and laminar distribution in the agranular and granular cortices. DA afferents were densest in the anterior cingulate (area 24) and the motor areas (areas 4, 6, and supplementary motor area [SMA]). In the latter they displayed a trilaminar pattern of distribution, predominating in layers I, IIIa, and V-VI, with characteristic cluster-like formations in layer IIIa, especially in the medial part of motor areas. In the granular prefrontal (areas 46, 9, 10, 11, 12), parietal (areas 1, 2, 3, 5, 7), temporal (areas 21, 22), and posterior cingulate (area 23) cortices, DA afferents were less dense and showed a bilaminar pattern of distribution, predominating in the depth of layer I and in layers V-VI; density in layers II, III, and IV was only 20% of that in layer I. The lowest density was in the visual cortex, particularly in area 17, where the DA afferents were almost restricted to layer I. The density of 5-HT innervation was generally greater than that of DA except in the motor areas and in the anterior cingulate cortex. Region-specific laminar patterns characterized (1) motor areas where a lower density in layer III contrasted with the clusters of DA axons in the same layer; (2) the primary visual cortex (area 17), where two bands of higher density in layers III-IV and layer V outlined a poorly innervated zone in layer IVc-beta; (3) the peristriate area 18, where the 5-HT network was relatively loose but with a denser band in layer III. Thus, DA innervation of the cerebral cortex displays major differences between rodents and primates, characterized by expanded cortical targets and by a highly differentiated laminar distribution.(ABSTRACT TRUNCATED AT 400 WORDS)

Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: A comparative study

“…This observation was previously made in humans, with the suggestion that this pattern could have evolutionary implications (Gaspar et al, 1989). This pattern of sublaminar innervation in the molecular layer has been reported in agranular cortices of long-tailed macaque monkeys (Berger et al, 1988), but may have been extended in humans to include both agranular and granular cortices (Gaspar et al, 1989). …”

“…A detailed analysis that included long-tailed macaques (Macaca fascicularis) and squirrel monkeys (Saimiri sciureus) did not report the presence of TH-ir coils within the cortical mantle (Lewis et al, 1987). Another study of Macaca fascicularis reported "clusters" of DAergic fibers in the upper portion of layer III of the motor areas 4 and 6, but not in other cortical areas (Berger et al, 1988). Similarly, we did not find any coil-like TH-stained structures in the frontal cortex of any species of Old World monkeys that we examined, whereas coils were consistently present in great apes.…”

Comparison of population activity in the dorsal premotor cortex and putamen during the learning of arbitrary visuomotor mappings

“…This signal was found in PMd in the present study (Figs. 3,4 and 6), and its properties supported the possibility that it reflects inputs from dopaminergic cells, perhaps those projecting directly to PMd (Lewis et al, 1987;Berger et al, 1988;Gaspar et al, 1992;Williams and Goldman-Rakic, 1993). If so, then blockade of dopamine receptors at the cortical level should eliminate this signal.…”

Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

“…However, reasonable candidates include dopaminergic (DA) neurons in the ventral tegemental area (VTA) and the substantia nigra pars compacta (SNc) that might influence activity in visual cortex via direct projections to early areas of visual cortex (Berger et al 1988(Berger et al , 1991Devoto and Flore 2006). However, these projections are generally thought to be sparse, so it is likely that indirect DA signals relayed through the striatum and then to frontal and parietal cortex play an important role in regulating value-related changes in early visual cortex (Barraclough et al 2004;Ding and Hikosaka 2006;Dorris and Glimcher 2004;Gläscher et al 2009;Glimcher 2003;Hikosaka et al 2008;Hollerman and Schultz 1998;Ikeda and Hikosaka 2003;Lau and Glimcher 2007;Leon and Shadlen 1999;Luk and Wallis 2009;Platt and Glimcher 1999;Schultz and Dickinson 2000;Seo et al 2007;Sugrue et al 2004;Wallis and Miller 2003;Watanabe 1996).…”