Neuroanatomy of the grey seal brain: bringing pinnipeds into the neurobiological study of vocal learning

Abstract

Comparative animal studies of complex behavioural traits, and their neurobiological underpinnings, can increase our understanding of their evolution, including in humans. Vocal learning, a potential precursor to human speech, is one such trait. Mammalian vocal learning is under-studied: most research has either focused on vocal learning in songbirds or its absence in non-human primates. Here, we focus on a highly promising model species for the neurobiology of vocal learning: grey seals ( Halichoerus grypus ). We provide a neuroanatomical atlas (based on dissected brain slices and magnetic resonance images), a labelled MRI template, a three-dimensional model with volumetric measurements of brain regions, and histological cortical stainings. Four main features of the grey seal brain stand out: (i) it is relatively big and highly convoluted; (ii) it hosts a relatively large temporal lobe and cerebellum; (iii) the cortex is similar to that of humans in thickness and shows the expected six-layered mammalian structure; (iv) there is expression of FoxP2 present in deeper layers of the cortex; FoxP2 is a gene involved in motor learning, vocal learning, and spoken language. Our results could facilitate future studies targeting the neural and genetic underpinnings of mammalian vocal learning, thus bridging the research gap from songbirds to humans and non-human primates. Our findings are relevant not only to vocal learning research but also to the study of mammalian neurobiology and cognition more in general. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Report on the brain of the monk seal (Monachus monachus, Hermann, 1779)

“…The rostral position of the cruciate sulcus observed in the monk seal is present also in the California sea lion, although on a more flat frontal pole (Figure 3). This feature is typical of carnivores and even more so in pinnipeds as reported in the literature (Fish, 1896;Hoeksema et al, 2021;Howell, 1928;Langworthy et al, 1938;Rioch, 1937). The longitudinal direction of the sulci was particularly evident in the temporal and occipital lobes of the monk seal.…”

“…Macroscopic observations indicate that the shape of the brain is remarkably similar to that of other Pinnipeds with some differences from Carnivora , for the general pattern of the gyri and marked piriform lobe (Hoeksema et al., 2021; Montie et al., 2009; Walløe et al., 2010). There are although, remarkable differences in the shape of the cortex between the California sea lion and the Mediterranean monk seal (Figures 1–3).…”

Vocal plasticity in harbour seal pups

“…To date, there is no evidence for direct cortico-bulbar projections for these specific neurons in any mammalian species except for humans. Our behavioural results lead to the prediction that harbour seals would be prime candidates among mammals to show direct anatomical connectivity between the laryngeal motor cortex and laryngeal motoneurons, as seen in humans [ 81 , 87 ].…”

“…As a complement to behavioural experiments, anatomical work could investigate the elastic properties of seal larynges to establish upper and lower anatomical boundaries for f 0 production [ 50 , 88 ]. Finally, neurobiological work should track purported direct cortico-laryngeal connections in seal pups, and compare them against closely related Caniformia not capable of f 0 plasticity [ 78 , 87 ].…”

Vocal learning in animals and humans

“…However, in many bird and mammal species, because of the complexity of the question under study and behaviour involved, the neurscientific basis of vocal learning remains unknown. Hoeksema et al [33] provide detailed information on the fine structure of the grey seal brain. This neuroanatomical atlas reveals that grey seals have a comparatively large temporal lobe and cerebellum, and that the cortex is similar to that in humans in thickness and shows the expected sixlayered mammalian structure.…”