Anatomical analysis of an aye-aye brain (Daubentonia madagascariensis, primates: Prosimii) combining histology, structural magnetic resonance imaging, and diffusion-tensor imaging.

This report presents initial results of a multimodal analysis of tissue volume and microstructure in the brain of an aye-aye (Daubentonia madagascariensis). The left hemisphere of an aye-aye brain was scanned using T2-weighted structural magnetic resonance imaging (MRI) and diffusion-tensor imaging (DTI) prior to histological processing and staining for Nissl substance and myelinated fibers. The objectives of the experiment were to estimate the volume of gross brain regions for comparison with published data on other prosimians and to validate DTI data on fiber anisotropy with histological measurements of fiber spread. Measurements of brain structure volumes in the specimen are consistent with those reported in the literature: the aye-aye has a very large brain for its body size, a reduced volume of visual structures (V1 and LGN), and an increased volume of the olfactory lobe. This trade-off between visual and olfactory reliance is likely a reflection of the nocturnal extractive foraging behavior practiced by Daubentonia. Additionally, frontal cortex volume is large in the aye-aye, a feature that may also be related to its complex foraging behavior and sensorimotor demands. Analysis of DTI data in the anterior cingulum bundle demonstrates a strong correlation between fiber spread as measured from histological sections and fiber spread as measured from DTI. These results represent the first quantitative comparison of DTI data and fiber-stained histology in the brain.

[1]  Thomas J Parsons,et al.  Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[2]  T. Ziehen Ueber die Grosshirnfurchung der Halbaffen und die Deutung einiger Furchen des menschlichen Gehirns , 1896, Archiv für Psychiatrie und Nervenkrankheiten.

[3]  Timothy Edward John Behrens,et al.  New approaches for exploring anatomical and functional connectivity in the human brain , 2004, Biological Psychiatry.

[4]  Ziheng Yang,et al.  Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context , 2004, Molecular ecology.

[5]  J. Allman,et al.  The scaling of frontal cortex in primates and carnivores. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  P. Sundgren,et al.  Diffusion tensor imaging of the brain: review of clinical applications , 2004, Neuroradiology.

[7]  David H. Laidlaw,et al.  Visualizing Diffusion Tensor MR Images Using Streamtubes and Streamsurfaces , 2003, IEEE Trans. Vis. Comput. Graph..

[8]  W. Jungers,et al.  The extinct sloth lemurs of Madagascar , 2003 .

[9]  J. Illes,et al.  Diffusion-tensor imaging of cognitive performance , 2002, Brain and Cognition.

[10]  P. Hüppi,et al.  Diffusion tensor imaging of normal and injured developing human brain ‐ a technical review , 2002, NMR in biomedicine.

[11]  M. Moseley Diffusion tensor imaging and aging – a review , 2002, NMR in biomedicine.

[12]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[13]  R L Winslow,et al.  Direct histological validation of diffusion tensor MRI in formaldehyde‐fixed myocardium , 2000, Magnetic resonance in medicine.

[14]  Anthony R. Ives,et al.  Using the Past to Predict the Present: Confidence Intervals for Regression Equations in Phylogenetic Comparative Methods , 2000, The American Naturalist.

[15]  Anthony R. Ives,et al.  An Introduction to Phylogenetically Based Statistical Methods, with a New Method for Confidence Intervals on Ancestral Values , 1999 .

[16]  E. Sterling,et al.  Tool Use, Aye-Ayes, and Sensorimotor Intelligence , 1999, Folia Primatologica.

[17]  Robert Barton,et al.  Comparative Primate Socioecology: The evolutionary ecology of the primate brain , 1999 .

[18]  John Forder,et al.  Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. , 1998, American journal of physiology. Heart and circulatory physiology.

[19]  C. Henriquez,et al.  Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. , 1998, American journal of physiology. Heart and circulatory physiology.

[20]  C. Beaulieu,et al.  Water diffusion in the giant axon of the squid: Implications for diffusion‐weighted MRI of the nervous system , 1994, Magnetic resonance in medicine.

[21]  E. Sterling,et al.  Dietary intake, food composition and nutrient intake in wild and captive populations of Daubentonia madagascariensis. , 1994, Folia primatologica; international journal of primatology.

[22]  A. Yoder Relative position of the Cheirogaleidae in strepsirhine phylogeny: a comparison of morphological and molecular methods and results. , 1994, American journal of physical anthropology.

[23]  C. Beaulieu,et al.  Determinants of anisotropic water diffusion in nerves , 1994, Magnetic resonance in medicine.

[24]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[25]  E. Simons The giant aye-aye Daubentonia robusta. , 1994, Folia primatologica; international journal of primatology.

[26]  E. Sterling Aye-ayes: specialists on structurally defended resources. , 1994, Folia primatologica; international journal of primatology.

[27]  C. J. Erickson,et al.  Tap-scanning and extractive foraging in aye-ayes, Daubentonia madagascariensis. , 1994, Folia primatologica; international journal of primatology.

[28]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[29]  M. Pagel A method for the analysis of comparative data , 1992 .

[30]  C. J. Erickson,et al.  Independent digit control in foraging by the aye-aye (Daubentonia madagascariensis). , 1991, Folia primatologica; international journal of primatology.

[31]  J. Ganzhorn,et al.  The aye-aye (Daubentonia madagascariensis) found in the eastern rainforest of Madagascar. , 1986, Folia primatologica; international journal of primatology.

[32]  Denis Le Bihan,et al.  Imagerie de diffusion in-vivo par résonance magnétique nucléaire , 1985 .

[33]  I. Tattersall The primates of Madagascar , 1982 .

[34]  H. Frahm,et al.  Comparison of brain structure volumes in Insectivora and Primates. I. Neocortex. , 1982, Journal fur Hirnforschung.

[35]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[36]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[37]  Sue Taylor Parker,et al.  Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in cebus monkeys and great apes , 1977 .

[38]  R. Bauchot,et al.  ENCÉPHALISATION ET NIVEAU ÉVOLUTIF CHEZ LES SIMIENS , 1969 .

[39]  C. J. Connolly,et al.  External morphology of the primate brain , 1950 .