1. Neuroscience

Between-species variation in neocortical sulcal anatomy of the carnivoran brain

  1. Magdalena Boch  Is a corresponding author
  2. Katrin Karadachka
  3. Kep-Kee Loh
  4. R Austin Benn
  5. Lea Roumazeilles
  6. Mads F Bertelsen
  7. Paul R Manger
  8. Ethan Wriggelsworth
  9. Simon Spiro
  10. Muhammad A Spocter
  11. Philippa J Johnson
  12. Kamilla Avelino-de-Souza
  13. Nina Patzke
  14. Claus Lamm
  15. Karla L Miller
  16. Jérôme Sallet
  17. Alexandre A Khrapitchev
  18. Benjamin C Tendler
  19. Rogier B Mars
  1. Oxford University Centre for Integrative Neuroimaging (OxCIN), FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
  2. Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Austria
  3. Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Netherlands
  4. Montreal Neurological Institute, McGill University, Canada
  5. Department of Psychology, National University of Singapore, Singapore
  6. Université Paris Cité, CNRS, Integrative Neuroscience and Cognition Center, France
  7. Copenhagen Zoo, Denmark
  8. School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, South Africa
  9. Zoological Society of London, United Kingdom
  10. Department of Anatomy, Des Moines University, United States
  11. Department of Clinical Sciences, Cornell College of Veterinary Medicine, Cornell University, United States
  12. Brazilian Neurobiodiversity Network, Physics Institute, Federal University of Rio de Janeiro, Brazil
  13. Department of Biological Science, Faculty of Sciences, Hokkaido University, Japan
  14. Faculty of Medicine, IMBB, HMU Health and Medical University, Germany
  15. Univ Lyon, Université Lyon 1, Inserm, Stem Cell and Brain Research Institute, France
  16. Department of Oncology, University of Oxford, United Kingdom
https://doi.org/10.7554/eLife.100851.3
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Cite this article
  1. Magdalena Boch
  2. Katrin Karadachka
  3. Kep-Kee Loh
  4. R Austin Benn
  5. Lea Roumazeilles
  6. Mads F Bertelsen
  7. Paul R Manger
  8. Ethan Wriggelsworth
  9. Simon Spiro
  10. Muhammad A Spocter
  11. Philippa J Johnson
  12. Kamilla Avelino-de-Souza
  13. Nina Patzke
  14. Claus Lamm
  15. Karla L Miller
  16. Jérôme Sallet
  17. Alexandre A Khrapitchev
  18. Benjamin C Tendler
  19. Rogier B Mars
(2026)
Between-species variation in neocortical sulcal anatomy of the carnivoran brain
eLife 13:RP100851.
https://doi.org/10.7554/eLife.100851.3
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6 figures, 1 table and 1 additional file

Figures

Figure 1
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Phylogeny of carnivoran sample.

The sample consists of species from both carnivoran sub-orders, Caniformia and Feliformia and includes members of eight different families (see also Table 1 in Materials and methods for a detailed sample description). The sub-order Caniformia includes Canidae and five Arctoidea families. All animals are terrestrial, except for the semi-aquatic Asian small-clawed otter. Phylogenetic relationships were derived from Field et al., 2022; Freedman et al., 2014; Kumar et al., 2017. k/mya, thousand/million years ago.

Figure 2 with 2 supplements
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Lateral view showing variation of sulcal patterns across carnivorans.

Surfaces are presented in descending order of sulcal complexity, starting with the canid brains that exhibited the highest number of unique major sulci. They are followed by felid brains which lacked the ectomarginal (orange, 4) and proreal (dark green, 11) sulcus but exhibited an additional diagonal (red, 13), and a split ectosylvian (brown, 2) sulcus, progressing towards species with the least complex sulcal topology. Despite exhibiting low sulcal complexity, the meerkat, Egyptian mongoose and striped hyaena had a caudal ectosylvian sulcus. The striped hyaena also exhibited a diagonal sulcus, analogous to Felids. All Arctoidea species in the fifth row, and the Asian small-clawed otter and red panda (sixth row, left) had complex or extended cruciate (light blue, 9), postcruciate (light green, 8) and ansate (purple red, 6) sulci. They also exhibited an inverted u-shaped suprasylvian sulcus compared to the arc shape observed in Canids and Felids (top four rows). We indicate the location of the cruciate sulcus with a blue dot if it is not well visible on the lateral surface due to its shape; see Figure 3 for a dorsal view. Anatomical locations are indicated on the dog surface in the top row, left corner. C, caudal; D, dorsal. ALI, Asiatic lion; ALE, Amur leopard; ASCO, Asian small-clawed otter; AWD, African wild dog; BB, brown bear; BD, bush dog; BEF, bat-eared fox; CA, caracal; DC, domestic cat; DD, domestic dog; DIN, dingo; EB, Eurasian badger; EL, Eurasian lynx; EMO, Egyptian mongoose; FER, ferret; FF, fennec fox; GW, grey wolf; JC, jungle cat; ME, meerkat; RAC, raccoon; RF, red fox; RP, red panda; SAC, South American coati; SC, sand cat; SHY, striped hyaena; TIG, Bengal tiger.

Figure 2—figure supplement 1
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Ventral view of major neocortical sulci.

The rostral and caudal rhinal fissure represent the ventral border of the carnivoran neocortex. The majority of the sulci visible on the ventral view can also be seen from a dorsal and/or lateral perspective (Figures 2 and 3), and the retrosplenial and occipitotemporal sulcus extend ventrally from the medial wall (see Figure 3—figure supplement 1). The ventral lateromedial sulcus (5, pink) can only be seen on the ventral surface of the occipital lobe. We were not able to consistently identify this sulcus in all carnivoran species. Animal acronyms: ALI, Asiatic lion; ALE, Amur leopard; ASCO, Asian small-clawed otter; AWD, African wild dog; BB, brown bear; BD, bush dog; BEF, bat-eared fox; CA, caracal; DC, domestic cat; DD, domestic dog; DIN, dingo; EB, Eurasian badger; EL, Eurasian lynx; EMO, Egyptian mongoose; FER, ferret; FF, fennec fox; GW, grey wolf; JC, jungle cat; ME, meerkat; RAC, raccoon; RF, red fox; RP, red panda; SAC, South American coati; SC, sand cat; SHY, striped hyaena; TIG, Bengal tiger.

Figure 2—figure supplement 2
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Lateral and ventral view of major neocortical sulci in additional individuals and sub-species.

The sulcal topology of the additional individuals closely resembled the surfaces presented in the main text, with all major sulci present (see Figure 2, Figure 2—figure supplement 1). Only minor variations in sulcal shape were observed. (A) For example, u-shaped pseudo-sylvian fissure (cyan, 1) of the second red panda was continuous in contrast to the split configuration observed in the other specimen (Figure 2). (B) Similar to both brown bear specimens, the marginal sulcus of the second grey wolf was also visible from the ventral view. In contrast, this sulcus was not visible in the ventral view of the first grey wolf or in any of the other species examined. Animal acronyms: DD, domestic dog; GW, grey wolf; SC, sand cat; PLE, Persian leopard; UBB, Ussuri brown bear; RP, red panda.

Figure 3 with 2 supplements
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Dorsal view reveals varying complexity of sulci in parietal and frontal cortices across carnivoran families.

Surfaces are presented in descending order of sulcal complexity, starting with brains exhibiting the most complex sulcal topology and progressing to those with the least, as in Figure 2. Only the wolf-like Canids (top row) and the bush dog (second row, left) had a proreal sulcus (green, 7). The brown bear had a secondary cruciate sulcus (light blue, 10). Anatomical locations are indicated on the domestic dog surface in the top row, left corner. Lat, lateral; C, caudal; RH, right hemisphere. ALI, Asiatic lion; ALE, Amur leopard; ASCO, Asian small-clawed otter; AWD, African wild dog; BB, brown bear; BD, bush dog; BEF, bat-eared fox; CA, caracal; DC, domestic cat; DD, domestic dog; DIN, dingo; EB, Eurasian badger; EL, Eurasian lynx; EMO, Egyptian mongoose; FER, ferret; FF, fennec fox; GW, grey wolf; JC, jungle cat; ME, meerkat; RAC, raccoon; RF, red fox; RP, red panda; SAC, South American coati; SC, sand cat; SHY, striped hyaena; TIG, Bengal tiger.

Figure 3—figure supplement 1
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Major neocortical sulci in the medial wall.

The cruciate sulcus (light blue, 1) was the only sulcus that was also visible on the lateral and dorsal view (see Figures 2 and 3). All species had a cruciate, splenial (purple red, 2), and retrosplenial (yellow, 3) sulcus. Occurrence and appearance of the suprasplenial (green, 4) and occipitotemporal (purple, 5) sulci varied across species. Anatomical locations are indicated on the domestic dog surface in the top row, left corner. R, rostral; D, dorsal. Animal acronyms: ALI, Asiatic lion; ALE, Amur leopard; ASCO, Asian small-clawed otter; AWD, African wild dog; BB, brown bear; BD, bush dog; BEF, bat-eared fox; CA, caracal; DC, domestic cat; DD, domestic dog; DIN, dingo; EB, Eurasian badger; EL, Eurasian lynx; EMO, Egyptian mongoose; FER, ferret; FF, fennec fox; GW, grey wolf; JC, jungle cat; ME, meerkat; RAC, raccoon; RF, red fox; RP, red panda; SAC, South American coati; SC, sand cat; SHY, striped hyaena; TIG, Bengal tiger.

Figure 3—figure supplement 2
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Dorsal and medial view of major neocortical sulci in additional individuals and sub-species.

None of the supplementary samples revealed major variations in shape or presence of the sulcus; only minor variations in sulcal shape were observed. (A) For example, in the Ussuri brown bear (UBB), the ansate sulcus (purple, 9) was more clearly identifiable than in the brown bear, as it displayed the typical perpendicular orientation relative to the marginal sulcus. (B) In the second sand cat, the cruciate (light blue, 1) and splenial (purple red, 2) sulci were detached, a variation also observed in several other species (Figure 3—figure supplement 2) whereas in the first sand cat, these sulci were merged. Animal acronyms: DD, domestic dog; GW, grey wolf; SC, sand cat; PLE, Persian leopard; UBB, Ussuri brown bear; RP, red panda.

Figure 4
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Sulcal anatomy variations and corresponding gyral differences.

As illustrated on the lateral view of the domestic dog brain (upper left corner), only Canidae have an ectomarginal gyrus (dark blue). Additionally, Canidae and Felidae (Asiatic lion, upper right corner) species have an (incomplete) sylvian gyrus (yellow). Species exhibiting a more complex postcruciate sulcus have an expanded postcruciate gyrus (light red) as illustrated on the South American coati brain (lower left corner). Nomenclature follows prior descriptions in Canidae and Felidae (Czeibert et al., 2019; Pakozdy et al., 2015; Rogers Flattery et al., 2023; Stolzberg et al., 2017), and descriptions of the ferret brain for species lacking an ectosylvian sulcus (Radtke-Schuller, 2018). The rostral suprasylvian gyrus (red) is also called the coronal gyrus in ferrets, and in the field of paleoneurology, post- and precruciate gyri (light red, purple) are often referred to as the posterior and anterior sigmoid gyrus (see e.g., Lyras et al., 2023). White space indicates allocortex. C, caudal; D, dorsal.

Figure 5 with 1 supplement
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Lineage-specific observations and potential functional correlates.

(A) The Arctoidea species with complex sulcal configurations in the somatosensory cortex also exhibit more pronounced forepaw dexterity (see e.g., Iwaniuk et al., 1999; Iwaniuk and Whishaw, 1999; Radinsky, 1968). In the red panda, coati, and raccoon, this potentially expanded cortical territory surrounding the postcruciate sulcus or complex appears to accommodate the primary somatosensory cortex, with a significant representation of the forepaw (see Figure 6). (B) Canids had the most complex occipitotemporal sulcal anatomy, followed by felids and the herpestids and striped hyaena with a unique sulcal configuration. This might indicate the expansion of auditory and visual regions in canids and of auditory regions in felids (see Figure 6). Arctoidea species exhibited the least complex occipitotemporal sulcal topology. (C) All canids with strong social bonds and that engage in cooperative hunting (Macdonald and Sillero-Zubiri, 2004; Wilson and Mittermeier, 2009; Wilson, 2000) had an additional sulcus in the frontal lobe, the proreal sulcus. Complementary quantitative analyses confirmed a positive association between sociality and proreal sulcus length, and between forepaw dexterity and the length of the postcruciate and cruciate sulci (Figure 5—figure supplement 1).

Figure 5—source data 1

Effects of forepaw dexterity and sociality on relative length of the proreal sulcus.

https://cdn.elifesciences.org/articles/100851/elife-100851-fig5-data1-v1.docx
Figure 5—source data 2

Effects of forepaw dexterity and sociality on relative length of the postcruciate sulcus.

https://cdn.elifesciences.org/articles/100851/elife-100851-fig5-data2-v1.docx
Figure 5—source data 3

Effects of forepaw dexterity and sociality on relative length of the cruciate sulcus.

https://cdn.elifesciences.org/articles/100851/elife-100851-fig5-data3-v1.docx
Figure 5—figure supplement 1
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Proportion of significant associations between relative sulcal length and behavioural characteristics.

Preliminary quantitative analyses, conducted to complement qualitative descriptions (Figure 5), reveal that the relative length of the proreal sulcus was consistently greater in cooperatively hunting species than in solitary hunters regardless of choice for reference sulcus (n = 7) and both hemispheres, while no effect of forepaw dexterity was observed (Figure 5—source data 1). In contrast, analyses of the postcruciate sulcus revealed the opposite pattern, with consistently greater sulcal length in species with high forepaw dexterity across all reference sulci (n = 4) and in both hemispheres, and no significant relationship with sociality (Figure 5—source data 2). Analyses of the cruciate sulcus length (n = 4 reference sulci) revealed a positive relationship with high forepaw dexterity in 75% of models in each hemisphere, but no significant relationship with sociality (Figure 5—source data 3). RH, right hemisphere; LH, left hemisphere.

Figure 6
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Schematic overview of cortical sulcal anatomy and available information about cortical sensory areas.

While knowledge of the sensory regions in carnivoran brains is still limited, the best-understood brains of the species in our sample were the domestic cat (third row, left) and ferret (bottom row, right) followed by the domestic dog (top row, left). Based on prior electrophysiological, histological, and neuroimaging research (e.g., Boch et al., 2021; Chengetanai et al., 2020a; Douglas Jameson et al., 1968; Guran et al., 2024; Hardin et al., 1968; Johnson et al., 2016; Kosmal, 2000; Law et al., 1988; Manger et al., 2002; Mclaughlin et al., 1998; Radtke-Schuller et al., 2020; Stolzberg et al., 2017; Tunturi, 1944; Welker and Campos, 1963), we indicate approximate locations of unimodal sensory cortices on a lateral view of the brains of these species. Darker shades indicate primary sensory cortices, including the primary visual (V1, yellow), auditory (A1, pink), motor (M1), and somatosensory (S1) cortex. Lighter shades mark higher-order unimodal sensory regions. White spaces indicate that these regions have not been investigated yet, or research to date has revealed inconclusive results. It is, for example, possible that the African wild dog has additional auditory regions located ventral to those identified (Chengetanai et al., 2020a). C, caudal; D, dorsal. Sulcus acronyms: an, ansate; co, coronal; cr, cruciate; di, diagonal; em, ectomarginal; enm, endomarginal; es, ectosylvian; ma, marginal; pr, postcruciate; pro, proreal; ps, pseudo-sylvian; ss, suprasylvian; tri, triradiate. Animal acronyms: ALI, Asiatic lion; ALE, Amur leopard; ASCO, Asian small-clawed otter; AWD, African wild dog; BB, brown bear; BD, bush dog; BEF, bat-eared fox; CA, caracal; DC, domestic cat; DD, domestic dog; DIN, dingo; EB, Eurasian badger; EL, Eurasian lynx; EMO, Egyptian mongoose; FER, ferret; FF, fennec fox; GW, grey wolf; JC, jungle cat; ME, meerkat; RAC, raccoon; RF, red fox; RP, red panda; SAC, South American coati; SC, sand cat; SHY, striped hyaena; TIG, Bengal tiger.

Tables

Table 1
Overview carnivoran brain collection.
Common nameSub-orderFamilyGenusSpeciesSexAgeScan protocolSource
Red pandaCanAiluridaeAilurusfulgensfANarrow, 7T2
Red pandaaCanAiluridaeAilurusfulgensfANarrow, 7T7
DingoCanCanidaeCanisdingouANarrow, 7T1
Domestic dogbCanCanidaeCanisfamiliarisfANarrow, 7T6
Domestic dogCanCanidaeCanisfamiliarisn/an/aWide, 3T9
American wolfCanCanidaeCanislupusfAWide, 7T1
European wolfaCanCanidaeCanislupusmSAWide, 7T1
African wild dogCanCanidaeLycaonpictusmAWide, 7T1
Bat-eared foxCanCanidaeOtocyonmegalotisfAWide, 3T8
Bush dogCanCanidaeSpeothosvenaticusfANarrow, 7T1
Red foxCanCanidaeVulpesvulpesmS/ANarrow, 7T4
Fennec foxCanCanidaeVulpeszerdamS/ANarrow, 7T4
Asian small-clawed otterCanMustelidaeAonyxcinereusmANarrow, 7T1
Eurasian badgerCanMustelidaeMelesmelesfANarrow, 7T2
FerretCanMustelidaeMustelaputoriusuuNarrow, 7T7
South American coatiCanProcyonidaeNasuanasuamSANarrow, 7T1
RaccoonCanProcyonidaeProcyonlotormAWide, 3T5
Brown bearCanUrsidaeUrsusArctos (arctos)fSAWide, 7T1
Ussuri brown bearaCanUrsidaeUrsusarctos (lasiotus)fSAWide, 3T5
CaracalFelFelidaeCaracalcaracaluuNarrow, 7T7
Domestic catcFelFelidaeFeliscatusfSAWide, 3T3
Jungle catFelFelidaeFelischausuuNarrow, 7T7
Sand catFelFelidaeFelismargaritauuNarrow, 7T7
Arabic sand cataFelFelidaeFelismargarita (harrisoni)fAWide, 3T8
Eurasian lynxFelFelidaeLynxlynxmANarrow, 7T2
Asiatic lionFelFelidaePantheraleofSAWide, 7T1
Amur leopardFelFelidaePantherapardus (orientalis)mSAWide, 7T1
Persian leopardaFelFelidaePantherapardus (tulliana)uuWide, 3T7
Bengal tigerFelFelidaePantheratigrisuuWide, 3T7
Egyptian mongooseFelHerpestidaeHerpestesichneumonuuNarrow, 7T7
MeerkatFelHerpestidaeSuricatasuricattamANarrow, 7T2
Striped hyaenaFelHyenidaeHyaenahyaenauuNarrow, 7T7

  1. Note. All animals are adults, n = 14 species belong to the Carnivoran sub-order Feliformia (Fel), and n = 16 are Caniformia (Can) species. Overall, our sample comprises eight different Carnivoran families. All data, except for the domestic cat, are post-mortem samples, and data were obtained from multiple sources: 1 = Copenhagen Zoo specimen collection, 2 = the Zoological Society of London, 3 = the Cornell University College of Veterinary Medicine, 4 = St. Louis Zoological Gardens, 5 = Hokkaido University (Hokkaido, Japan), 6 = donated by a private owner, 7 = Mammalian MRI (MaMI) database (Assaf et al., 2020), 8 = Lyon Comparative Brain Collection acquired by J.S. and colleagues, 9 = stereotactic breed-averaged template (Johnson et al., 2020). Data was collected with wide-bore scanners, typically used for human neuroimaging, or narrow-bore scanners, typically used for rodent neuroimaging. Field strength of the scanners was either 3 or 7 tesla (T; see scan protocol). aFor consistency, we only labelled one specimen in the main study, marked (sub-)species are added for supplementary analyses. bThe domestic dog sample is a Belgian shepherd; we also created a surface from a stereotactic breed-averaged template (Johnson et al., 2020) for supplementary confirmatory analysis. cThe domestic cat sample is a domestic shorthair cat. f, female; m, male; u, unknown; A, adult; SA, subadult; S/A, adult or subadult.

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  1. Magdalena Boch
  2. Katrin Karadachka
  3. Kep-Kee Loh
  4. R Austin Benn
  5. Lea Roumazeilles
  6. Mads F Bertelsen
  7. Paul R Manger
  8. Ethan Wriggelsworth
  9. Simon Spiro
  10. Muhammad A Spocter
  11. Philippa J Johnson
  12. Kamilla Avelino-de-Souza
  13. Nina Patzke
  14. Claus Lamm
  15. Karla L Miller
  16. Jérôme Sallet
  17. Alexandre A Khrapitchev
  18. Benjamin C Tendler
  19. Rogier B Mars
(2026)
Between-species variation in neocortical sulcal anatomy of the carnivoran brain
eLife 13:RP100851.
https://doi.org/10.7554/eLife.100851.3