Anatomical Specializations for Nocturnality in a Critically Endangered Parrot, the Kakapo (Strigops habroptilus)

The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds

Autoradiographic quantification of muscarinic cholinergic synaptic markers in bat, shrew, and rat brain

We employed radioligand binding autoradiography to determine the distributions of pre- and postsynaptic cholinergic radioligand binding sites in the brains of two species of bat, one species of shrew, and the rat. High affinity choline uptake sites were measured with [ 3 H]hemicholinium, and presynaptic cholinergic vesicles were identified with [ 3 H]vesamicol. Muscarinic cholinergic receptors were determined with [ 3 H]scopolamine. The distribution patterns of the three cholinergic markers were similar in all species examined, and identified known major cholinergic pathways on the basis of enrichments in both pre- and postsynaptic markers. In addition, there was excellent agreement, both within and across species, in the regional distributions of the two presynaptic cholinergic markers. Our results indicate that pharmacological identifiers of cholinergic pathways and synapses, including the cholinergic vesicle transport site, and the organizations of central nervous system cholinergic pathways are phylogenetically conserved among eutherian mammals.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/45409/1/11064_2004_Article_BF00971334.pd

Functional anatomy of forebrain vocal control pathways in the budgerigar (Melopsittacus undulatus)

Budgerigars throughout life are capable of learning to produce many different sounds including those of human speech. Like humans, budgerigars use multiple craniomotor systems and coordinate both orosensory and auditory feedback in specialized forebrain nuclei. Although budgerigar auditory-vocal learning has a different evolutionary origin from that of human speech, both the human and budgerigar systems can control F0 and can alter the distribution of energy in spectral bands by adjusting the filter properties of the vocal tract. This allows budgerigars to produce an extremely diverse array of calls including many broadband and highly complex sounds

Cytoarchitecture of vocal control nuclei in nestling budgerigars: Relationships to call development

Changes in the cytoarchitecture of vocal control nuclei were investigated in nestling budgerigars (Melopsittacus undulatus) from hatching to fledging (five to six weeks) in relation to changes in vocalizations produced by nestlings during this period. The nuclei investigated were the hypoglossal nucleus, dorsomedial nucleus of the intercollicular midbrain, central nucleus of the archistriatum, central nucleus of the lateral neostriatum, oval nucleus of the hyperstriatum ventrale, medial division of the oval nucleus of the anterior neostriatum, and magnocellular nucleus of the lobus parolfactorius. These nuclei have been shown to form functional circuits in adults related to vocal learning. Consistent with previously reported results, we found that call development could be described in terms of five different phases based on changes in the duration and segmentation of single and multiple segment foodbegging calls and the appearance of the first socially learned contact calls around the time of fledging. We also found that call segment duration exhibited an inverted U-shaped developmental function during the nestling period, as has been found for total call duration. Cytoarchitectonic studies revealed striking changes in the cellular architecture of vocal control nuclei during the first four weeks posthatching. At hatching the hypoglossal nucleus exhibits adult-like cytoarchitecture, and the central nucleus of the archistriatum and the central nucleus of the lateral neostriatum are distinguishable from surrounding fields. By one week posthatch, the central nucleus of the archistriatum exhibits an adult-like appearance, while other telencephalic vocal control nuclei do not exhibit adult-like cytoarchitecture until three to four weeks posthatching. By two weeks posthatching, the dorsomedial nucleus of the intercollicular midbrain also exhibits adult-like cytoarchitecture. We observed substantial decreases in the thickness of ventricular proliferation zones during this period, with decreases in ventricular zones occurring at about the same point that nuclei at corresponding levels come to exhibit adult-like cytoarchitectonic features. Of interest is the fact that cytoarchitectural development occurs asynchronously in different brain regions, with the appearance of adult-like characteristics in the hindbrain and midbrain occurring before the appearance of adult-like cytoarchitectonic characteristics in telencephalic nuclei. These results are consistent with recent lesion studies indicating that neither auditory feedback nor telencephalic vocal control nuclei are necessary for the production of foodbegging and other nestling calls until three to four weeks posthatching

Core and Shell Song Systems Unique to the Parrot Brain.

The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot "core" song system is similar to the song systems of songbirds and hummingbirds, whereas the "shell" song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities