Diffusion tractography reveals pervasive asymmetry of cerebral white matter tracts in the bottlenose dolphin (Tursiops truncatus)

Abstract

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 provides a unique opportunity to examine asymmetries of brain structure and function. In the present study, diffusion tensor imaging and tractography were used to investigate cerebral white matter asymmetry in the bottlenose dolphin (Tursiops truncatus). Widespread white matter asymmetries were observed with the preponderance of tracts exhibiting leftward structural asymmetries. Leftward lateralization may reflect differential processing and execution of behaviorally variant sensory and motor functions by the cerebral hemispheres. The arcuate fasciculus, an association tract linked to human language evolution, was isolated and exhibited rightward asymmetry suggesting a right hemisphere bias for conspecific communication unlike that of most mammals. This study represents the first examination of cetacean white matter asymmetry and constitutes an important step toward understanding potential drivers of structural asymmetry and its role in underpinning functional and behavioral lateralization in cetaceans.

Keywords: Arcuate fasciculus; Asymmetry; Bottlenose dolphin (Tursiops truncatus); Diffusion tensor imaging (DTI); Tractography; White matter.

Fig. 1

a Anterior, b posterior, c dorsal, d ventral, e left parasagittal, and f right parasagittal views of the T. truncatus cerebral surface (translucent dark gray) and underlying white matter tracts of the anterior thalamic radiation (red), arcuate fasciculus (rose), cingulum (light green), corticocaudate tract (orange), external capsule (dark green), forceps minor of the corpus callosum (yellow), fornix (fuchsia), and superior longitudinal fasciculus system (light blue). Color designations are consistent across figures; however, the superior longitudinal fasciculus system in Fig. 3 reflects parcellation of the sub-tracts, SLF I, SLF II, and SLF III

Fig. 2

Left and right parasagittal views of the T. truncatus cerebral surface (translucent dark gray) and underlying white matter tracts of the association fiber system, including the arcuate fasciculus, cingulum, and external capsule. Color designations are consistent across figures

Fig. 3

Left and right parasagittal views of the T. truncatus cerebral surface (translucent dark gray) and underlying associative superior longitudinal fasciculus system, comprising sub-tracts SLF I, SLF II, and SLF III. Color designations within the superior longitudinal fasciculus system reflect parcellation of sub-tracts SLF I, SLF II, and SLF III

Fig. 4

Left and right parasagittal views of the T. truncatus cerebral surface (translucent dark gray) and underlying white matter tracts of the projection fiber system, including the anterior thalamic radiation, corticocaudate tract, and fornix. Color designations are consistent across figures

Fig. 5

Left and right parasagittal views of the T. truncatus cerebral surface (translucent dark gray) and underlying corpus callosum of the commissural fiber system. Color designations are consistent across figures

Fig. 6

a Total volume (mm³, purple) and relative volume (%) for each tract (left, black; right, red) and b total fiber number (purple) and relative fiber number (%) for each tract (left, black; right, red). Left and right tracts combined represent 100% of the total volume or total fiber number. ARC arcuate fasciculus, ATR anterior thalamic radiation, CCA corticocaudate tract, CG cingulum, EC external capsule, SLF superior longitudinal fasciculus system, SLF I superior longitudinal fasciculus I, SLF II superior longitudinal fasciculus II, SLF III superior longitudinal fasciculus III

Fig. 7

Lateralization index (LI) for the volume, fiber number, and mean fiber length of the arcuate fasciculus (ARC, rose), anterior thalamic radiation (ATR, red), corticocaudate tract (CCA, orange), cingulum (CG, light green), external capsule (EC, dark green), superior longitudinal fasciculus system (SLF, light blue), superior longitudinal fasciculus I (SLF I, dark blue), superior longitudinal fasciculus II (SLF II, light purple), and superior longitudinal fasciculus III (SLF III, dark purple). Tract-specific LI values for each measurement are shown in parentheses on the right. Color designations are consistent across figures; however, the superior longitudinal fasciculus system in Fig. 3 reflects parcellation of the sub-tracts, SLF I, SLF II, and SLF III