Anatomical and volumetric description of the guiana dolphin (Sotalia guianensis) brain from an ultra-high-field magnetic resonance imaging

Abstract

The Guiana dolphin (Sotalia guianensis) is a common species along Central and South American coastal waters. Although much effort has been made to understand its behavioral ecology and evolution, very little is known about its brain. The use of ultra-high field MRI in anatomical descriptions of cetacean brains is a very promising approach that is still uncommon. In this study, we present for the first time a full anatomical description of the Guiana dolphin's brain based on high-resolution ultra-high-field magnetic resonance imaging, providing an exceptional level of brain anatomical details, and enriching our understanding of the species. Brain structures were labeled and volumetric measurements were delineated for many distinguishable structures, including the gray matter and white matter of the cerebral cortex, amygdala, hippocampus, superior and inferior colliculi, thalamus, corpus callosum, ventricles, brainstem and cerebellum. Additionally, we provide the surface anatomy of the Guiana dolphin brain, including the labeling of main sulci and gyri as well as the calculation of its gyrification index. These neuroanatomical data, absent from the literature to date, will help disentangle the history behind cetacean brain evolution and consequently, mammalian evolution, representing a significant new source for future comparative studies.

Keywords: Brain evolution; Comparative neuroanatomy; Dolphin brain; MRI.

Fig. 1

a Stranded adult female Guiana dolphin from Baía de Sepetiba, Rio de Janeiro, Brazil. The body length is 174 cm, b Guiana dolphin brain in a plastic bag filled with sodium azide phosphate buffer prior to MRI scanning

Fig. 2

A Manual tracings for exposed (yellow), pial (blue), and GM/WM interface (pink) perimeters. Note that the pial surface areas include cortical sulci and gyri whereas the external contours do not. Scale bar = 1 cm, B Manual tracing of the callosal boundaries on the most midsagittal section of the Guiana dolphin brain. The cc area was the average of three measurements for the section (blue, pink, and yellow). Scale bar = 2 cm

Fig. 3

External aspects of the Guiana dolphin fresh brain in frontal (A), lateral (B), dorsal (C), ventral (D), and mid-sagittal (E) views. Scale bar = 1 cm. Anatomical directions: D (dorsal), V (ventral), R (rostral), and C (caudal). For other abbreviations see list

Fig. 4

Coronal magnetic resonance imaging (MRI) scans of the Guiana dolphin brain at 1.9mm interval—from anterior to posterior axis; T2 weighted; MRI grayscale inverted. Scale bar = 2 cm. Top left: Illustration of the position of the brain in the sagittal plane. For abbreviations see list

Fig. 4

Coronal magnetic resonance imaging (MRI) scans of the Guiana dolphin brain at 1.9mm interval—from anterior to posterior axis; T2 weighted; MRI grayscale inverted. Scale bar = 2 cm. Top left: Illustration of the position of the brain in the sagittal plane. For abbreviations see list

Fig. 5

Sagittal magnetic resonance imaging (MRI) scans of the Guiana dolphin brain at 1.9 mm interval—from to axis; T2 weighted; MRI grayscale inverted. Scale bar = 2 cm. Top left: Illustration of the position of the brain in the horizontal plane. In the bottom, the midsagittal cerebellar section demonstrates the lobules and arborization patterns of the vermis of the structure. Cerebellar lobules are labeled in white, and sulci are labeled in yellow. For abbreviations see list

Fig. 6

Horizontal magnetic resonance imaging (MRI) scans of the Guiana dolphin brain at 1.9 mm interval—from to axis; T2 weighted; MRI grayscale inverted Scale bar = 2 cm. Top left: Illustration of the position of the brain in the sagittal plane. For abbreviations see list

Fig. 7

a When regressing the square root of the corpus callosum area against the cubic root of brain mass derived from other cetaceans (blue dots; exponent of 0.946 ± 0.049 r² = 0.85; p < 0.0001; Manger et al. 2010), the Guiana dolphin (*g) falls slightly below the 95% prediction interval for the group with an exponent of 0.956 ± 0.049; r² = 0.85; p < 0.0001, having smaller than the expected cross-sectional area of the corpus callosum for its brain mass, b when regressing the gyrification index (GI) against the brain mass calculated derived from other cetaceans, the Guiana dolphin and all other cetaceans lie above the GI regression described for carnivores, artiodactyls, and primates (black line and dots; Manger et al. 2012). However, the Guiana dolphin's GI also falls substantially below the data points of other cetaceans (blue line; 0.019 ± 0.018; r² = 0.215; p < 0.0003; data from Manger, 2012), making it an outlier when compared to both cetaceans and other mammals, c when regressing the hippocampus area against the brain volume, the Guiana dolphin (*g) falls well within the 95% prediction interval established for all the other cetaceans (exponent of (0.553 ± 0.168; r² = 0.55; p = 0.0131; re-plotted from Patzke et al. 2015). The relationship that describes the regression of the hippocampus against brain volume for all the other non-cetacean mammals (black line) is better characterized by an exponential curve (red dashed lines), d when regressing the amygdala volume against the brain volume, the guiana dolphin (*g) falls well within the 95% prediction interval described from the regression derived for cetaceans, with an exponent of 0.813 ± 0.042 (blue line; r² = 0.99; p < 0.0001), falling below the regression derived for all the other non-cetacean mammals (black line; exponent of 0.713 ± 0.005; r ² = 0.98; p < 0.0001; Patzke et al. 2015), e when regressing the cerebellum volume against the brain volume, the Guiana dolphin (*g) falls well within the 95% prediction interval derived from this regression for other cetaceans with an exponent of 1.003 ± 0.033 (r.² = 0.981; p = 0.0001; data from Marino et al. ; Maseko et al. ; Schwerdtfeger et al. 1984). In comparison to other mammals (primates, megachiropterans, and insectivores), cetaceans—including the Guiana dolphin—have larger than expected cerebellar volumes according to brain mass (data from Stephan et al. ; Baron et al. ; Schwerdtfeger et al. ; Marino et al. 2000), f When regressing the ventricular volume against the brain volume, the Guiana dolphin (*g) falls within the range described for other mammals (megachiropterans, microchiropterans, and insectivores; data from Stephan et al. ; Baron et al. 1996)