A comparative analysis of the dopaminergic innervation of the executive caudal nidopallium in pigeon, chicken, zebra finch, and carrion crow

Abstract

Despite the long, separate evolutionary history of birds and mammals, both lineages developed a rich behavioral repertoire of remarkably similar executive control generated by distinctly different brains. The seat for executive functioning in birds is the nidopallium caudolaterale (NCL) and the mammalian equivalent is known as the prefrontal cortex (PFC). Both are densely innervated by dopaminergic fibers, and are an integration center of sensory input and motor output. Whereas the variation of the PFC has been well documented in different mammalian orders, we know very little about the NCL across the avian clade. In order to investigate whether this structure adheres to species-specific variations, this study aimed to describe the trajectory of the NCL in pigeon, chicken, carrion crow and zebra finch. We employed immunohistochemistry to map dopaminergic innervation, and executed a Gallyas stain to visualize the dorsal arcopallial tract that runs between the NCL and the arcopallium. Our analysis showed that whereas the trajectory of the NCL in the chicken is highly comparable to the pigeon, the two Passeriformes show a strikingly different pattern. In both carrion crow and zebra finch, we identified four different subareas of high dopaminergic innervation that span the entire caudal forebrain. Based on their sensory input, motor output, and involvement in dopamine-related cognitive control of the delineated areas here, we propose that at least three morphologically different subareas constitute the NCL in these songbirds. Thus, our study shows that comparable to the PFC in mammals, the NCL in birds varies considerably across species.

Event-related functional MRI of awake behaving pigeons at 7T

“…In addition, further pallial areas that receive dopaminergic input were strongly activated, such as amygdala, hippocampus, striatum, and pallidum 50 . We also observed BOLD responses in the NCL, the avian functional analog to the prefrontal cortex 51 . The dopaminergic input to NCL 51 activates D1 receptors of principal neurons 52 .…”

“…We also observed BOLD responses in the NCL, the avian functional analog to the prefrontal cortex 51 . The dopaminergic input to NCL 51 activates D1 receptors of principal neurons 52 . In pigeons, D1A and D1D receptors mediate learning of stimulus-response associations 53 .…”

Dopamine D1 receptor activation drives plasticity in the songbird auditory pallium

“…Dopaminergic fibers permeate the secondary auditory regions NCM and the caudomedial mesopallium (CMM), but not the thalamo-recipient auditory region, Field L (Reiner et al, 1994; von Eugen et al, 2020). Dopamine receptor mRNA maps onto this architecture, such that D1 receptors (D1Rs) are abundant in NCM and CMM, and D2 receptors are abundant in CMM but not in NCM.…”

Connectivity between nidopallium caudolateral and visual pathways in color perception of zebra finches

“…Primate or human studies reveal that the visual associated telencephalon communicates with higher order of brain areas, such as the prefrontal cortex [29][30][31] . In pigeons, the nidopallium caudolateral (NCL) is equivalent to the prefrontal cortex in mammals [32][33][34] . NCL in pigeon executes functions such as planning and decision-making 33,34 .…”

“…In chickens, NCL also involve in imprinting behavior 35 . Recently, a study indicates that the location and trajectory of NCL are species-specific; the patterns of dopaminergic innervations are strikingly different between pigeons/chickens and zebra finches 32 . These findings imply that the zebra finch's NCL may modulate different functions than those of pigeons/chickens.…”