Synopsis

Brain enlargement is associated with concomitant growth of interneuronal distance, increased conduction time, and reduced neuronal interconnectivity. Recognition of these functional constraints led to the hypothesis that large-brained mammals should exhibit greater structural and functional brain lateralization. As a taxon with the largest brains in the animal kingdom, Cetacea (whales, dolphins, and porpoises) provide a unique opportunity to examine asymmetries of brain structure and function. In the present study, diffusion tensor imaging (DTI) and tractography were used to investigate cerebral white matter asymmetry in the bottlenose dolphin.

Introduction

Asymmetries of brain structure and function are found throughout the vertebrates¹, varying in type and magnitude. A lateralized brain is characterized by anatomical or functional differences between its bilateral components, (cerebral hemispheres, cortical areas, cerebral white matter tracts). It has been hypothesized that the extent of brain lateralization increases with increasing brain size^2,3 to 1) avoid extreme and untenable brain enlargement consequent to the maintenance of complete neuronal interconnectivity (i.e., the number of neurons in which an individual neuron is directly connected), and 2) mitigate increased interhemispheric conduction delay due to longer transmission distances. Constraints on interconnectivity and conduction time inherent to the evolution of large brains may impose strict limits on global processing and favor local processing leading to the development of brain lateralization. A high degree of lateralization would be expected in cetaceans, which have the largest brains in the animal kingdom ^2,3. Indeed, structural and functional brain lateralization has been observed throughout the Cetacea. An example of this is unihemispheric sleep, important for the maintenance of locomotion, surface respiration, and vigilance by one cerebral hemisphere, while simultaneously permitting sleep in the contralateral hemisphere^8-12.Despite these observations no previous studies have investigated lateralized white matter tract asymmetry in Cetacea. The present study examines the extent of cerebral white matter tract asymmetry in the bottlenose dolphin. DTI and tractography were used for the identification, measurement, and 3D reconstruction of white matter tracts of the association, projection, and commissural fiber systems

Methods

The specimen was a formalin-fixed brain of a captive 27-year-old male bottlenose dolphin. The brain was removed and fixed within 3 hours of death. Data was acquired using a GE 3.0 T Signa 750 MRI. DTI was acquired in the axial plane using single-shot EPI, 60 direction diffusion-encoding, b value 3000 s/mm², six non-diffusion weighted images (b₀), slice thickness 3 mm, TR 8 s, TE 82 ms, 4 averages, matrix 128 × 128 mm, FOV 200 mm, 56 axial slices, and voxel size 0.78 × 0.78 × 3 mm. 3 Nex. Total scan time 105 minutes. Axial T2 anatomical images were also acquired. DTI data was concatenated and eddy currents corrected using FSL. Data were fit to a diffusion model for each voxel using the FMRIB Diffusion Toolbox¹³ (FDT). FA, M_D, A_D, and R_D maps were calculated. The FA and the main eigenvector maps were imported into DtiStudio for fiber tracking analysis. Fiber tracking was performed using the FACT method¹⁴. Tracking was terminated when the local FA fell below the FA threshold of 0.1, or when the tract-turning angle exceeded the angular threshold of 55^o. A multiple ROI approach was used to reconstruct cerebral white matter tracts using FA maps. Eight white matter tracts were reconstructed. Measurements of the volume, voxel size¹⁵, fiber number¹⁶, mean fiber length¹⁶, FA , M_D , A_D, and R_D¹⁷ were acquired for each tract. Asymmetries of each tract-specific measurement were assessed by calculating the lateralization index (LI)¹⁸. Calculations of the relative volume and relative fiber number were performed for each tract to determine the percentage of the total volume or total fiber number occupied by the left and right tracts.

Results

The anterior thalamic radiation, arcuate fasciculus, cingulum, corticocaudate tract, external capsule, forceps minor of the corpus callosum, fornix, superior longitudinal fasciculus system, and the sub-tracts of the superior longitudinal fasciculus system (SLF I, SLF II, and SLF III) were reconstructed. Asymmetries were found for the relative volume relative fiber number, and lateralization index for most of the tracts examined (see figures 2 and 3). The absence of lateralization for FA, M_D, A_D, and R_D in all of the tracts examined suggests that the tract-specific measurements were not confounded by these parameters, and were indeed asymmetric in certain tracts. Moreover, symmetry of microstructural diffusion parameters and uniformity of the structural dataset indicate that macrostructural asymmetries were not due to tissue damage or incomplete fixation of the specimen.

Discussion and Conclusion

These findings suggest widespread structural asymmetries of cerebral white matter in this dolphin, and provide support for the hypothesis that large brains should exhibit pronounced lateralization. Moreover, the sparse reconstruction of the corpus callosum in parallel with various reports on the diminutive size of the cetacean corpus callosum relative to the volume of the cerebral hemispheres^19-24 correspond to observations and predictions of reduced interhemispheric connectivity with brain enlargement. The observation of this pervasive asymmetry in cerebral white matter architecture is proposed to reflect differential perception, processing, and production of social and nonsocial sensory signals and motor actions in the bottlenose dolphin.

Acknowledgements

No acknowledgement found.

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