Interspecies avian brain chimeras reveal that large brain size differences are influenced by cell-interdependent processes.

Chun-Chun Chen,Erich D Jarvis,Evan Balaban

doi:10.1371/journal.pone.0042477

Chun-Chun Chen, Erich D Jarvis + Show 1 more

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https://doi.org/10.1371/journal.pone.0042477

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Abstract

Like humans, birds that exhibit vocal learning have relatively delayed telencephalon maturation, resulting in a disproportionately smaller brain prenatally but enlarged telencephalon in adulthood relative to vocal non-learning birds. To determine if this size difference results from evolutionary changes in cell-autonomous or cell-interdependent developmental processes, we transplanted telencephala from zebra finch donors (a vocal-learning species) into Japanese quail hosts (a vocal non-learning species) during the early neural tube stage (day 2 of incubation), and harvested the chimeras at later embryonic stages (between 9–12 days of incubation). The donor and host tissues fused well with each other, with known major fiber pathways connecting the zebra finch and quail parts of the brain. However, the overall sizes of chimeric finch telencephala were larger than non-transplanted finch telencephala at the same developmental stages, even though the proportional sizes of telencephalic subregions and fiber tracts were similar to normal finches. There were no significant changes in the size of chimeric quail host midbrains, even though they were innervated by the physically smaller zebra finch brain, including the smaller retinae of the finch eyes. Chimeric zebra finch telencephala had a decreased cell density relative to normal finches. However, cell nucleus size differences between each species were maintained as in normal birds. These results suggest that telencephalic size development is partially cell-interdependent, and that the mechanisms controlling the size of different brain regions may be functionally independent.

Highlights

Comparative analyses have suggested that relative brain size differences among species correlate with behavioral complexity [1,2,3]
The quail tectal cell numbers in the chimeras were not significantly different from normal quails (Figure 11E). These findings indicate that the quail host had a significant effect on accelerating cell density changes in the zebra finch ventricular zone and telencephalon, and increasing the number of cells in the zebra finch telencephalon; but the finch donor only had a small influence on the cell density in the quail optic tectum
We found that the proportional sizes of the lateral forebrain bundle (LFB), containing the fiber tracts that go between graft and host, showed no significant group differences at either ED9 (Figure 12A) or ED12 (Figure 12B)

Summary

Introduction

Comparative analyses have suggested that relative brain size differences among species correlate with behavioral complexity [1,2,3]. Proportional enlargements of particular brain regions or pathways are thought to give rise to enhanced behavioral capacities for abilities that are influenced by those brain regions. Such modifications of brain structure have generally been related to broad patterns of evolutionary specialization within particular vertebrate groups, such as hippocampal size and spatial memory in food-storing birds, tectal size and visual acuity differences among avian species, and cortical regional size differences and the complexity of social behaviors in both primate and fish species [2,4,5,6,7,8,9,10,11,12]. All three groups have evolved a disproportionately large adult telencephalon relative to the average vertebrate, and this increased size is thought to be due at least in part to additional circuitry responsible for song and speech learning, and/or to an associated increase in size of other brain regions involved in communicative, social and cognitive abilities [2,6,20,21]

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