The prefrontal cortex of the bottlenose dolphin (Tursiops truncatus Montagu, 1821): a tractography study and comparison with the human

Abstract

Cetaceans are well known for their remarkable cognitive abilities including self-recognition, sound imitation and decision making. In other mammals, the prefrontal cortex (PFC) takes a key role in such cognitive feats. In cetaceans, however, a PFC could up to now not be discerned based on its usual topography. Classical in vivo methods like tract tracing are legally not possible to perform in Cetacea, leaving diffusion-weighted imaging (DWI) as the most viable alternative. This is the first investigation focussed on the identification of the cetacean PFC homologue. In our study, we applied the constrained spherical deconvolution (CSD) algorithm on 3 T DWI scans of three formalin-fixed brains of bottlenose dolphins (Tursiops truncatus) and compared the obtained results to human brains, using the same methodology. We first identified fibres related to the medio-dorsal thalamic nuclei (MD) and then seeded the obtained putative PFC in the dolphin as well as the known PFC in humans. Our results outlined the dolphin PFC in areas not previously studied, in the cranio-lateral, ectolateral and opercular gyri, and furthermore demonstrated a similar connectivity pattern between the human and dolphin PFC. The antero-lateral rotation of the PFC, like in other areas, might be the result of the telescoping process which occurred in these animals during evolution.

Keywords: Brain evolution; CSD; Cetacean; DWI; Dolphin; PFC.

Fig. 1

Neocortical brain map of a human in left view, b human (left hemisphere) and dolphin (right hemisphere) in dorsal view and c dolphin in left view. Dark blue, Motor cortex; light blue, premotor cortex; Red, somatosensory cortex; light red, associative somatosensory cortex; yellow, V1; light yellow, associative visual cortex; dark green, A1; light green, associative auditory cortex; orange, PFC. Cr cruciate sulcus, Cs central sulcus, En entolateral sulcus, ES ectosylvian gyrus, Es ectosylvian sulcus, La lateral sulcus, LG lateral gyrus, PRG precentral gyrus, PSG postcentral gyrus, Sf Sylvian fissure, SS suprasylvian gyrus, Ss suprasylvian sulcus. Neocortical maps adapted from Martin (; human) and Cozzi et al. (, dolphin)

Fig. 2

Representation of the MDN mask based on the panels descripted by Kruger (1959) and Morgane and Jacobs (1972). The directions from a to c are rostro-caudal with a 3D visualisation of the section and the whole mask at the correspondent plane; a section taken based on panel number 6; b section taken based on panel number 7; c section taken based on panel number 3

Fig. 3

Prefrontal pathways in the dolphin and human brains. a Tracts generated from seeding the MDN (blue shape) in dolphin. b Tracts generated from seeding MDN (blue shape) in human. CC corpus callosum, En entolateral sulcus, Es ectolateral sulcus, ES ectolateral gyrus, La lateral sulcus, LG lateral gyrus, Sf sylvian fissure, Ss suprasylvian sulcus, SS suprasylvian gyrus. Red scale bar = 5 cm

Fig. 4

Putative PFC (red mask) based on previous projections from the MD (blue mask). a Frontal view; b dorsal view

Fig. 5

Prefrontal pathways in the dolphin and human brains. a Tracts generated from seeding the PFC (red shape) in dolphin. b Tracts generated from seeding PFC (red shape) in human. The MDN is represented in blue. CA caudate nucleus, CC corpus callosum, CI cingulum, En entolateral sulcus, Es ectolateral sulcus, ES ectolateral gyrus, La lateral sulcus, LG lateral gyrus, PU putamen, SLF superior longitudinal fasciculus, Ss suprasylvian sulcus, SS suprasylvian gyrus. Red scale bar = 5 cm

Fig. 6

Constrained tractography between the putative found PFC (red shape) and the MDN (blue shape). CA caudate nucleus, Cr cruciate sulcus, En entolateral sulcus, Es ectolateral sulcus, ES ectolateral gyrus, La lateral sulcus, LG lateral gyrus, PU putamen, Sf sylvian fissure, Ss suprasylvian sulcus, SS suprasylvian gyrus

Fig. 7

Constrained tractography between the putative found PFC (red shape) and the MDN (blue shape). CC corpus callosum

Fig. 8

Approximate PFC representation (orange area) in human (A) and dolphin (B) brain. For abbreviations, see the list. Red scale bar = 5 cm

Fig. 9

Schematic picture of the brain evolution from its “initial” form (top, Glezer et al. 1988) to the dolphin (Jacobs et al. ; Cozzi et al. 2017) and human (Martin 2021) brains (bottom). Orange, PFC; Blue, SSC; Red, MC; Green, A1/A2; Yellow, V1/V2. Sf, Sylvian fissure. Dashed purple line delimits the border of the insular cortex. The dotted arrow in the human brain indicates the displacement of the other areas due to the expansion of the PFC. The dotted arrows in the dolphin brain indicate the rotation of the organ around the insular cortex and the probable cranio-lateral shift of the PFC and other cortical areas on the surface. X, Y body axes