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 telesco** process which occurred in these animals during evolution.
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Introduction
The bottlenose dolphin Tursiops truncatus (Montagu, 1821) is a member of the Delphinidae family often kept in captivity, and consequently frequently studied. Individuals of this species may perform a large variety of complex cognitive tasks including sound imitation, understanding of human syntax, conceptual decision taking, understanding numerosity, and self-recognition (Kilian et al. 2003; Kuczaj et al. 2015, 2016), corrected from Gibb’s ringing artefacts (Kellner et al. 2015), corrected for EPI-distortion (Holland et al. 2010), b0-field inhomogeneity (Andersson et al. 2003; Smith et al. 2004), Eddy-current and movement (Andersson and Sotiropoulos 2016). Subsequently, the dhollander algorithm was applied to compute different response functions for the white matter (WM, anisotropic), cerebrospinal fluid and grey matter (CSF and GM, both isotropic). Finally, the fibre orientation distribution (FOD) was calculated before the elaboration of the tractography (Dhollander et al. 2016a, b, 2017; Tournier et al. 2019). Each brain was then investigated individually.
Humans
Preprocessed data of human brains were already present in the HCP files, but further steps were added in order to create a template atlas, averaging all five subjects. Images were corrected form bias field and group DWI intensity normalisation was performed. In these data, there were 4 shells, therefore, the dhollander algorithm was used to estimate different response functions and then average them to calculate the FOD. Once all subjects’ FOD were complete, we created a population template, a template mask and war** all the FOD images to the template space (for reference, see Tournier et al. 2019).
Tractography
Throughout the following, the procedure was applied to both right and left hemispheres. In dolphins, the MDN mask was manually drawn using the ITK-SNAP software (Yushkevich et al. 2016; www.itksnap.org; version 3.8.0) following the topographical location described by Kruger (1959) and Morgane and Jacobs (1972). The thalamic subdivision is quite evident in the histological data if compared to our MRI data. We first identified the thalamic topographic position based on the histology, and then drew the areas. Since the slides did not include all the thickness of the thalamus, we tried to reconstruct the missing space following its shape (Fig. 2). The final mask was intentionally slightly eroded to avoid the generation of erroneous extra fibres. Since there is no map of the PFC location in Cetacea, a PFC area was first created, based from the tracts originating from the MDN. To verify that the tracts were not artefactual, we restricted the tracking using the designated PFC as the seed image and reaching the MDN nucleus, thus restraining the fibres to the bundle only connecting one with the other.
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
In the human, MDN and PFC were manually drawn with ITK-SNAP, based on the currently available templates and atlases (Tamraz and Comair 2000; Cho 2010; Ding et al. 2016). For both dolphin and human brains, fibre tracking was performed through a deterministic algorithm based on CSD, with the FOD file as input and the following parameters: FA threshold 0.1 for dolphin brains (as they were fixed) and 0.2 for human brains (since the subjects were alive), step size 0.1 mm, default angle threshold 60°, and default streamline count (5000).
Results
Seeding point: MDN nuclei
In the dolphin brains, the main fibre bundles exiting the MDN were directed cranially running below the cruciate sulcus (Cr) towards the ventro-cranial pole, passing between the Putamen (PU) and caudate nucleus (CA). Other consistent fibre bundles went dorsally following the internal capsule and terminated in i) the supralimbic cortex around the entolateral sulcus (En), the lateral sulcus (La), and the suprasylvian sulcus (Ss); then ii) laterally in the temporal lobes around the ectolateral sulcus (Es). Some tracts ran caudally to the Edinger–Westphal nucleus (EW), the Interstitial Nucleus of Cajal (INC) and the elliptic nucleus (NE), then moved ventrally towards the crus cerebri (Fig. 2a). Projections from the MDN were also commonly distributed within the thalamus and then ran to other brain areas. Few aberrant fibres passed through the superior colliculi (SC) (Fig. 3a).
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
In the human brain, fibres ran to the PFC following the anterior thalamic peduncle, then went laterally to the temporal lobe following the inferior thalamic peduncle. Some of the latter fibres split from the inferior thalamic bundle to join the optic radiation directed towards the parietal lobe. We also noted fibres that reached the CC to spread in the contralateral hemisphere (Fig. 3b).
Thanks to our previous results, we were able to estimate a presumptive frontal region based on the extension of the fibres on the WM tracts (Fig. 4).
Seeding point: acquired PFC
Seeding the putative PFC resulted in the presence of several ipsilateral U-shaped fibres within the area. Other fibre tracts were oriented towards the basal ganglia and the cingulate cortex (CI). Other bundles continued through the MDN to end in the pons. A consistent number of fibres joined the superior longitudinal fasciculus (SLF) directed to the temporal lobe (Es, Ss) while others arose to En and La (Fig. 5a). Finally, some tracts reached the CC and crossed contralaterally.
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
In the human brain, ipsilateral fibres created from the PFC joined the inferior fronto-occipital fasciculus and reached the V1. Other fibres joined the fornix, then ran caudally towards the MDN, the CI. Some tracts were directed to the temporal lobe apparently through the SLF. Fibres directed towards the mesencephalon reached the periaqueductal grey and the red nucleus in the tegmentum (Fig. 5b). Finally, consistent fibre bundles moved to the CC and then crossed to the contralateral hemisphere.
Specifically constrained thalamo-cortical connections
To delimit the fibres previously generated singularly from the MDN nuclei or from the presumptive PFC, we also selectively constrained the tracking between these two regions.
In general, these fibres were fewer and more limited. In the dolphin, cortically seeded bundles passed below the Cr and between the basal ganglia to reach the MDN. Other streamlines ran laterally to the temporal lobe (Ss, Es), and very few fibres continued dorsally to the ENs and LAs. Finally, some fibre bundles were directed caudally to the red nucleus and the elliptic nucleus (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
Prefrontal pathways in the human brain between PFC and MDN also crossed through the CC and reached the temporal lobe of the contralateral hemisphere through the inferior thalamic peduncle. Few fibres detached from the inferior thalamic peduncle and continued caudally until the VC (Fig. 7).
Discussion
A precise identification of the topography and connectivity of the PFC (or its homologue) in dolphins represents a consistent step forward towards the understanding of their brain architecture and the neural basis for some of the complex behaviours of the species. To the best of our knowledge, DWI technique is currently one of the very few technically feasible and ethically acceptable approaches to identify the PFC in dolphins, and potentially other large ex-vivo brains.
In the present study, we performed CSD-based tractography and aimed at identifying fibre tracts that connect selected thalamic nucleus to their related cortical targets/origin. We then compared the data with those obtained in the human brain. Since the human PFC is one of the key areas assigned to higher brain functions (Tranel et al. 2003; Butler and Hodos 2005; Kandel et al. 2021), we searched for an area in the dolphin brain with the same characteristic connections.
CSD is a HARDI algorithm of DWI that, within the limits of human clinical MRI parameters, can reconstruct crossing fibres within a voxel, thus giving a more plausible biological result (Arrigo et al. 2016; Jeurissen et al. 2017). The algorithm can be applied and extended also to fixed brains, much like with DTI (D’Arceuil and de Crespigny 2007; Rane and Duong 2011; Gerussi et al. 2022). Classical retrograde and anterograde tract-tracing remains the gold standard methodology to accurately study brain connections. However, the technique was seldom performed in cetacean brains, and likely will not be in the future because of the ethical constraints briefly outlined in the Introduction. In this context, opportunistic fixed-brain DWI (and its various algorithmic variations), therefore, constitutes an adequate method to investigate brain connections in these mammals, even considering its biases and limits to interpretation (Jeurissen et al. 2017; Schilling et al. 2020). Fixation produces microstructural changes such as dehydration or tissue degeneration, which in turn may alter some MRI parameters including SNR, FA and apparent diffusion coefficient (ADC) (D’Arceuil and de Crespigny 2007; Rane and Duong 2011). Therefore, the obtained results must consider all the limitations of DWI in general and DWI applied to fixed tissues.
Tracing and tractography in dolphins and porpoises
Literature on evoked potential placed the bottlenose dolphin V1/V2 around En in the LG, extending rostro-caudally and with the La as its lateral boundary. A1/A2 develops from there along the SS, reaching the Ss with a rostro-caudal direction (for review see Supin et al. 2001). According to the literature, the Cr separates rostrally the medial SSC from the lateral MC. Other reports that used tracing in the harbour porpoise (Phocoena phocoena) established the existence of projections from the parvocellular part of the MGN to the suprasylvian and ectosylvian gyri (Krashnoshchekova and Figurina 1980; Voronov et al. 1985), and the involvement of the LGN as target of the optic nerve. Evoked potentials were used also for track-tracing-based injections in various areas of the neocortex (LG, the SS, ES, temporal and orbital) of the harbour porpoise (Revishchin and Garey 1990). Overall, the data obtained showed that medial thalamic projections progressively crossed to a lateral cortical position, therefore, ending contralaterally to their origin (see Revishchin and Garey 1990, Fig. 13). However, no tracing study was ever performed on a putative PFC.
A recent DTI study described for the first time the existence of a direct auditory pathway from IC to MGN to the temporal lobe near the Sylvian fissure in the common (Delphinus delphis) and pantropical spotted dolphin (Stenella attenuata), and an overlap of thalamic visual and auditory pathways (Berns et al. 2015). Such direct pathways, often hypothesised, but never demonstrated before, suggest a direct and profound interconnection of the dolphin visual and auditory system. Nevertheless, given the extremely limited data concerning the functional auditory region in cetaceans, it should be considered a still partially unsolved scientific question.
Topography and characterisation of the PFC in the human and dolphin brain
The human PFC can be divided into four functional areas: orbitofrontal cortex (OFC), dorsolateral PFC (dlPFC), dorsomedial PFC (dmPFC) and ventromedial PFC (vmPFC) (Kolb 2015). The caudolateral boundaries of the PFC roughly correspond to the cranial part of the precentral sulcus (premotor cortex) and medially to the cingulate cortex. The Brodmann areas overlap** the human PFC are: BA8-14, 24, 25, 32, 44–47 (Murray et al. 2017). These are marked by notable cytoarchitectural differences that determine their boundaries (Brodmann’s 2006; Petrides and Pandya 2012). Although the frontal lobe possess its own cytoarchitectural peculiarity (Hof et al. 2005), there are no such characteristic differences in the bottlenose dolphin, and other cetaceans in general (Kern et al. 2011; van Kann et al. 2017). We started by identifying topographical landmarks that may characterise comparatively the dolphin PFC (see orange area in the Fig. 8) and then proceeded with CSD tractography. The average mass of the brain in the bottlenose dolphin is 1.550 g (Huggenberger et al. 2019), vs. the average value of 1300–1400 g for the human (Miller and Corsellis 1977) must be taken in account. Without discussing the body and brain weight correlation, or the Encephalization QuotientFootnote 1 (Jerison 1973; for discussion of its application to cetaceans see Cozzi et al. 2016), we emphasise that the position of the area occupied by the PFC, based on topographically equivalent landmarks, appears more lateral in the dolphin brain comparatively to man, even considering the different brain shape and dimensions.
Prefrontal pathways
In the human DWI scans, seeding the human MDN (Fig. 2b) resulted in fibres that reached most of the PFC through the anterior thalamic peduncle, while some other fibres joined the inferior thalamic peduncle and were then oriented towards the somatosensory association area in the parietal lobe and V1. Our results were consistent with those found by Grodd et al. (2020). When the same method was applied to the brains of the bottlenose dolphins, the resulting fibres joined the internal capsule, passed between the basal ganglia towards the ventro-cranial pole and ended ventrally to the Cr. Other fibres were directed towards either the LGN or the MGN, going through the internal capsule and terminating in the parietal lobe. We also noted that some fibres were directed caudally, possibly to merge in post-thalamic tectal pathways. A putative PFC could be identified in the bottlenose brain by map** fibres that reached the non-parietal neocortex (Fig. 8). The projections arising from this putative PFC then continued (a) within the PFC itself; (b) moved to the contralateral PFC through the CC; (c) to the CI; (d) to the pons passing between the basal ganglia and MDN; or (e) to the temporal lobe following the SLF. The connectivity pattern detected in the bottlenose brain was in fact similar to that found in the human brain.
To check whether these fibres were not just artefactual, we first seeded the MDN to establish where the fibres were going. Then we seeded the designated area to see if some of the fibres projected independently back to the MDN. We noticed that some fibres again connected the PFC with the MDN, but other bundles were oriented towards different areas. The PFC is a multimodal association area which receives and sends inputs to other brain regions, and—to this effect—our results were consistent with what reported in the literature (Fuster 2015). We finally constrained the seeding between the two areas to qualitatively see the amount of fibres only related to these seeds, and exclude other unspecific bundles. We found a more marked asymmetry in the dolphin brains compared to human brains (Figs. 6 and 7), but given the scope of our study and its qualitative approach, we did not emphasise this aspect.
The acquisition parameters used to scan the live human brains (referred to the HCP) were evidently better than those of the (dead) dolphin brains. However, we detected no substantial loss of signal in the formalin-fixed dolphin brains, so that identification of a putative PFC area in their brain gave results that were largely comparable to the human. No former tracking or injection studies based on evoked potential reported a functional identification of a putative PFC in dolphin, hence, this is the first report of a putative PFC in this species, and, to the best of our knowledge, in all cetaceans. Its boundaries start in the orbital lobe, extend laterally in the cranial ES and reach the cranial opercular lobe. However, additional fibres were connected to areas placed below the SSC and MC cortices, in which pyramidal neurons were previously found (Manger 2006).
According to the concept of the “initial brain” (for reference see Glezer et al. 1988, Fig. 7) modern mammals still retain some key topographical features already present in the brains of their early ancestors, notwithstanding the divergent evolutionary path of the taxa. The enlarged human neocortex contains far more and varied cortical modules than in primordial mammals. The cetacean brain obviously followed a different evolutionary route since the brain mantle greatly expanded to the uttermost known limits for mammals in terms of relative cortical size, while the cytoarchitecture is poorly differentiated and mostly homogeneous in the neocortex (Cozzi et al. 2017).
In the human brain, the development of the PFC displaced all the areas caudally, thus modifying the primeval topographical scheme (Fig. 9). In cetaceans, the progressive evolution to life in the water caused a wide range of body structure modifications. In the head specifically, the growth of the melon, the telesco** process, and the nasal shift which caused the change of the cranial axes and shape, might have prevailed over the longitudinal development of the brain (Miller 1923; Cozzi et al. 2017; Roston and Roth 2019). Consequently, the brain folded around the insula (see dotted arrows in Fig. 9) and expanded more laterally: what in terrestrial mammals is “caudal” becomes “dorsal” in the dolphin and so forth (Morgane and Jacobs 1972). Concomitant space limits within the cerebral cavity prompted a striking cortical gyrification and induced the topographical shift of neocortical areas. Our data based on CSD tractography confirmed that the (evolutionary) process that modified the cetacean brain was compatible with the persistence of a very large and richly connected PFC area.
Schematic picture of the brain evolution from its “initial” form (top, Glezer et al. 1988) to the dolphin (Jacobs et al. 1984; 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
The PFC of terrestrial mammals, and the correspondent areas in birds, are highly innervated by dopaminergic neurons (Sawaguchi and Goldman-Rakic 1991; Gaspar et al. 1992; Güntürkün 2005). Based on this neurochemical concept, further studies are needed to investigate the actual presence of dopaminergic neurons in the PFC of dolphins. This is particularly important in the fronto-ventral area, where one should not expect to find an associative cortex (Manger 2006, referring to Kojima 1951), and in the lateral (opercular) area. Additional functional MRI (fMRI) or recently developed functional near-infrared spectroscopy (fNIRS) techniques (Scholkmann et al. 2014) might also become useful for the study of brain functions through the proxy of increased blood flow during local stimulation, very similar to blood-oxygen-level-dependent contrast in fMRI. A composite multidisciplinary approach may eventually shed light on the unmapped cortical fields of these mammals with remarkable cognitive abilities.
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
Notes
EQ [EQ = Ei / 0.12 × P2/3; E.i = mean brain weight, P = mean body weight] is 3.79 in the bottlenose dolphin vs. 6.62 in man, according to Huggenberger et al. (2019)
Abbreviations
- En:
-
Entolateral sulcus
- Es:
-
Ectolateral sulcus
- La:
-
Lateral sulcus
- Sf:
-
Sylvian fissure
- Ss:
-
Suprasylvian sulcus
- AC:
-
Anterior commissure
- CC:
-
Corpus callosum
- Cl:
-
Cingulate cortex
- CSD:
-
Constrained spherical deconvolution
- DTI:
-
Diffusion tensor imaging
- DWI:
-
Diffusion-weighted imaging
- ES:
-
Ectolateral gyrus
- MC:
-
Motor cortex
- MDN:
-
Medio-dorsal thalamic nucleus
- MGN:
-
Medial geniculate nucleus
- LG:
-
Lateral gyrus
- LGN:
-
Lateral geniculate nucleus
- OT:
-
Optic tract
- PFC:
-
Prefrontal cortex
- SS:
-
Suprasylvian gyrus
- SSC:
-
Somatosensory cortex
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Acknowledgements
The authors thank the Human Connectom Project for the available data used in this manuscript. (Principal Investigators: Bruce Rosen, M.D., Ph.D., Arthur W. Toga, Ph.D., Van J. Weeden, M.D.). HCP funding was provided by the National Institute of Dental and Craniofacial Research (NIDCR), the National Institute of Mental Health (NIMH) and the National Institute of Neurological Disorders and Stroke (NINDS). HCP data are disseminated by the Laboratory of Neuro Imaging at the University of Southern California).
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Open access funding provided by Università degli Studi di Padova within the CRUI-CARE Agreement. This work was supported by a grant from the German Research Council to OG (Gu 227/16-1), and from the University of Padova D.O.R. Bruno Cozzi.
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Conceptualisation: TG, OG, BC; methodology: TG, MB, LS; formal analysis and investigation: TG, JMG, AP, SH, BC; writing—original draft preparation: TG; writing—review and editing: JMG, MB, LS, SH, OG, BC; funding acquisition: OG, BC; supervision: JMG, MB, LS, SH, OG, BC.
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The dolphin brains used in this study were sampled during routine necropsies at the University. Therefore, no animals were deliberately killed for the purpose of this study. The human scans were freely accessible on the Human Connectom Project website, under the condition of adding them in the acknowledgments.
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Gerussi, T., Graïc, JM., Peruffo, A. et al. The prefrontal cortex of the bottlenose dolphin (Tursiops truncatus Montagu, 1821): a tractography study and comparison with the human. Brain Struct Funct 228, 1963–1976 (2023). https://doi.org/10.1007/s00429-023-02699-8
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DOI: https://doi.org/10.1007/s00429-023-02699-8