Comparative neuroimaging of the carnivoran brain: Neocortical sulcal anatomy
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eLife Assessment
This useful study presents the first detailed and comprehensive description of brain sulcus anatomy of a range of carnivoran species based on a robust manual labeling model allowing species comparisons. Although the database is recognized and the method for reconstructing cortical surfaces is convincing, the evidence supporting the conclusions is incomplete due to the lack of appropriate quantitative measurements and analyses. Considering additional specimens to assess intraspecies variations, as well as exploring the functional correlates of interspecies differences would increase the scope of the study. Setting an instructive foundation for comparative anatomy, this study will be of interest to neuroscientists and neuroimaging researchers interested in that field, as well as in brain morphology and sulcal patterns, their phylogeny, and ontogeny in relation to functional development and behaviour.
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Abstract
Carnivorans are an important study object for comparative neuroscience, as they exhibit a wide range of behaviours, ecological adaptations, and social structures. Previous studies have mainly examined relative brain size, but a comprehensive understanding of brain diversity requires the investigation of other aspects of their neuroanatomy. Here, we obtained primarily post-mortem brain scans from eighteen species of the order Carnivora, reconstructed their cortical surfaces, and examined neocortical sulcal anatomy to establish a framework for systematic inter-species comparisons. We observed distinct regional variations in sulcal anatomy, potentially related to the species’ behaviour and ecology. Arctoidea species with pronounced forepaw dexterity exhibited complex sulcal configurations in the presumed somatosensory cortex but low sulcal complexity in the presumed visual and auditory occipitotemporal cortex. Canidae had the largest number of unique major sulci with a unique sulcus in the occipital cortex and highly social canids featuring an additional frontal cortex sulcus. We also observed differentially complex occipito-temporal sulcal patterns in Felidae and Canidae, indicative of changes in auditory and visual areas that may be related to foraging strategies and social behaviour. In conclusion, this study presents an inventory of the sulcal anatomy of a number of rarely studied carnivoran brains and establishes a framework and novel avenues for further investigations employing a variety of neuroimaging modalities to reveal more about carnivoran brain diversity.
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eLife Assessment
This useful study presents the first detailed and comprehensive description of brain sulcus anatomy of a range of carnivoran species based on a robust manual labeling model allowing species comparisons. Although the database is recognized and the method for reconstructing cortical surfaces is convincing, the evidence supporting the conclusions is incomplete due to the lack of appropriate quantitative measurements and analyses. Considering additional specimens to assess intraspecies variations, as well as exploring the functional correlates of interspecies differences would increase the scope of the study. Setting an instructive foundation for comparative anatomy, this study will be of interest to neuroscientists and neuroimaging researchers interested in that field, as well as in brain morphology and sulcal patterns, …
eLife Assessment
This useful study presents the first detailed and comprehensive description of brain sulcus anatomy of a range of carnivoran species based on a robust manual labeling model allowing species comparisons. Although the database is recognized and the method for reconstructing cortical surfaces is convincing, the evidence supporting the conclusions is incomplete due to the lack of appropriate quantitative measurements and analyses. Considering additional specimens to assess intraspecies variations, as well as exploring the functional correlates of interspecies differences would increase the scope of the study. Setting an instructive foundation for comparative anatomy, this study will be of interest to neuroscientists and neuroimaging researchers interested in that field, as well as in brain morphology and sulcal patterns, their phylogeny, and ontogeny in relation to functional development and behaviour.
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Reviewer #1 (Public review):
Summary:
The paper by Boch and colleagues, entitled Comparative Neuroimaging of the Carnivore Brain: Neocortical Sulcal Anatomy, compares and describes the cortical sulci of eighteen carnivore species, and sets a benchmark for future work on comparative brains.
Based on previous observations, electrophysiological, histological and neuroimaging studies and their own observations, the authors establish a correspondence between the cortical sulci and gyri of these species. The different folding patterns of all brain regions are detailed, put into perspective in relation to their phylogeny as well as their potential involvement in cortical area expansion and behavioral differences.
Strengths:
This is a pioneering article, very useful for comparative brain studies and conducted with great seriousness and based on …
Reviewer #1 (Public review):
Summary:
The paper by Boch and colleagues, entitled Comparative Neuroimaging of the Carnivore Brain: Neocortical Sulcal Anatomy, compares and describes the cortical sulci of eighteen carnivore species, and sets a benchmark for future work on comparative brains.
Based on previous observations, electrophysiological, histological and neuroimaging studies and their own observations, the authors establish a correspondence between the cortical sulci and gyri of these species. The different folding patterns of all brain regions are detailed, put into perspective in relation to their phylogeny as well as their potential involvement in cortical area expansion and behavioral differences.
Strengths:
This is a pioneering article, very useful for comparative brain studies and conducted with great seriousness and based on many past studies. The article is well-written and very didactic. The different protocols for brain collection, perfusion, and scanning are very detailed. The images are self-explanatory and of high quality. The authors explain their choice of nomenclature and labels for sulci and gyri on all species, with many arguments. The opening on ecology and social behavior in the discussion is of great interest and helps to put into perspective the differences in folding found at the level of the different cortexes. In addition, the authors do not forget to put their results into the context of the laws of allometry. They explain, for example, that although the largest brains were the most folded and had the deepest folds in their dataset, they did not necessarily have unique sulci, unlike some of the smaller, smoother brains.
Weaknesses:
The article is aware of its limitations, not being able to take into account inter-individual variability within each species, inter-hemispheric asymmetries, or differences between males and females. However, this does not detract from their aim, which is to lay the foundations for a correspondence between the brains of carnivores so that navigation within the brains of these species can be simplified for future studies. This article does not include comparisons of morphometric data such as sulci depth, sulci wall surface, or thickness of the cortical ribbon around the sulci.
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Reviewer #2 (Public review):
Summary:
The authors have completed MRI-based descriptions of the sulcal anatomy of 18 carnivoran species that vary greatly in behaviour and ecology. In this descriptive study, different sulcal patterns are identified in relation to phylogeny and, to some extent, behaviour. The authors argue that the reported differences across families reflect behaviour and electrophysiology, but these correlations are not supported by any analyses.
Strengths:
A major strength of this paper is using very similar imaging methods across all specimens. Often papers like this rely on highly variable methods so that consistency reduces some of the variability that can arise due to methodology.
The descriptive anatomy was accurate and precise. I could readily follow exactly where on the cortical surface the authors referring. …
Reviewer #2 (Public review):
Summary:
The authors have completed MRI-based descriptions of the sulcal anatomy of 18 carnivoran species that vary greatly in behaviour and ecology. In this descriptive study, different sulcal patterns are identified in relation to phylogeny and, to some extent, behaviour. The authors argue that the reported differences across families reflect behaviour and electrophysiology, but these correlations are not supported by any analyses.
Strengths:
A major strength of this paper is using very similar imaging methods across all specimens. Often papers like this rely on highly variable methods so that consistency reduces some of the variability that can arise due to methodology.
The descriptive anatomy was accurate and precise. I could readily follow exactly where on the cortical surface the authors referring. This is not always the case for descriptive anatomy papers, so I appreciated the efforts the authors took to make the results understandable for a broader audience.
I also greatly appreciate the authors making the images open access through their website.
Weaknesses:
Although I enjoyed many aspects of this manuscript, it is lacking in any quantitative analyses that would provide more insights into what these variations in sulcal anatomy might mean. The authors do discuss inter-clade differences in relation to behaviour and older electrophysiology papers by Welker, Campos, Johnson, and others, but it would be more biologically relevant to try to calculate surface areas or volumes of cortical fields defined by some of these sulci. For example, something like the endocast surface area measurements used by Sakai and colleagues would allow the authors to test for differences among clades, in relation to brain/body size, or behaviour. Quantitative measurements would also aid significantly in supporting some of the potential correlations hinted at in the Discussion.
Although quantitative measurements would be helpful, there are also some significant concerns in relation to the specimens themselves. First, almost all of these are captive individuals. We know that environmental differences can alter neocortical development and humans and nonhuman animals and domestication affects neocortical volume and morphology. Whether captive breeding affects neocortical anatomy might not be known, but it can affect other brain regions and overall brain size and could affect sulcal patterns. Second, despite using similar imaging methods across specimens, fixation varied markedly across specimens. Fixation is unlikely to affect the ability to recognize deep sulci, but variations in shrinkage could nevertheless affect overall brain size and morphology, including the ability to recognize shallow sulci. Third, the sample size = 1 for every species examined. In humans and nonhuman animals, sulcal patterns can vary significantly among individuals. In domestic dogs, it can even vary greatly across breeds. It therefore remains unclear to what extent the pattern observed in one individual can be generalized for a species let alone an entire genus or family. The lack of accounting for inter-individual variability makes it difficult to make any firm conclusions regarding the functional relevance of sulcal patterns.
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Author response:
eLife Assessment
This useful study presents the first detailed and comprehensive description of brain sulcus anatomy of a range of carnivoran species based on a robust manual labeling model allowing species comparisons. Although the database is recognized and the method for reconstructing cortical surfaces is convincing, the evidence supporting the conclusions is incomplete due to the lack of appropriate quantitative measurements and analyses. Considering additional specimens to assess intraspecies variations, as well as exploring the functional correlates of interspecies differences would increase the scope of the study. Setting an instructive foundation for comparative anatomy, this study will be of interest to neuroscientists and neuroimaging researchers interested in that field, as well as in brain morphology and …
Author response:
eLife Assessment
This useful study presents the first detailed and comprehensive description of brain sulcus anatomy of a range of carnivoran species based on a robust manual labeling model allowing species comparisons. Although the database is recognized and the method for reconstructing cortical surfaces is convincing, the evidence supporting the conclusions is incomplete due to the lack of appropriate quantitative measurements and analyses. Considering additional specimens to assess intraspecies variations, as well as exploring the functional correlates of interspecies differences would increase the scope of the study. Setting an instructive foundation for comparative anatomy, this study will be of interest to neuroscientists and neuroimaging researchers interested in that field, as well as in brain morphology and sulcal patterns, their phylogeny, and ontogeny in relation to functional development and behaviour.
We are pleased that our primary objective of creating a comprehensive framework to navigate carnivoran brains is considered as successfully achieved and that our work is expected to be of broad interest to various disciplines, as it provides the foundation for future investigations into carnivoran brain organization.
As we will set out below, a description of the major sulci is an appropriate measure for large-scale comparative anatomy — it is stable enough in the population of each species to not require a large N, provides a suitable variability across species, and can be related to other aspects of between-species diversity. We will include a number of additional species to increase the scope of the study, as suggested. Although a quantitative assessment of functional correlates is, in principle, beyond the scope of this first foundational paper, we will provide a first start of this as well. We emphasize, however, that this was a secondary outcome, emerging after first application of the framework.
Public Reviews:
Reviewer #1 (Public review):
Summary:
The paper by Boch and colleagues, entitled Comparative Neuroimaging of the Carnivore Brain: Neocortical Sulcal Anatomy, compares and describes the cortical sulci of eighteen carnivore species, and sets a benchmark for future work on comparative brains.
Based on previous observations, electrophysiological, histological and neuroimaging studies and their own observations, the authors establish a correspondence between the cortical sulci and gyri of these species. The different folding patterns of all brain regions are detailed, put into perspective in relation to their phylogeny as well as their potential involvement in cortical area expansion and behavioral differences.
Strengths:
This is a pioneering article, very useful for comparative brain studies and conducted with great seriousness and based on many past studies. The article is well-written and very didactic. The different protocols for brain collection, perfusion, and scanning are very detailed. The images are self-explanatory and of high quality. The authors explain their choice of nomenclature and labels for sulci and gyri on all species, with many arguments. The opening on ecology and social behavior in the discussion is of great interest and helps to put into perspective the differences in folding found at the level of the different cortexes. In addition, the authors do not forget to put their results into the context of the laws of allometry. They explain, for example, that although the largest brains were the most folded and had the deepest folds in their dataset, they did not necessarily have unique sulci, unlike some of the smaller, smoother brains.
Weaknesses:
The article is aware of its limitations, not being able to take into account inter-individual variability within each species, inter-hemispheric asymmetries, or differences between males and females. However, this does not detract from their aim, which is to lay the foundations for a correspondence between the brains of carnivores so that navigation within the brains of these species can be simplified for future studies. This article does not include comparisons of morphometric data such as sulci depth, sulci wall surface, or thickness of the cortical ribbon around the sulci.
We thank the reviewer for their overwhelmingly positive evaluation of our work. As noted by the reviewer, our primary aim was to establish a framework for navigating carnivoran brains to lay the foundation for future research. We are pleased that this objective is deemed as successfully achieved.
As the reviewer points out, we do not quantify within-species intraindividual differences. This is a conscious choice; we aimed to emphasize breadth of species over individuals, as is standard in large-scale comparative anatomy (cf. Heuer et al., 2023, eLife; Suarez et al., 2022, eLife). Following the logic of phylogenetic relationships, the presence of a particular sulcus in related species is also a measure of reliability. We felt safe in this choice, as previous work in both primates and carnivorans has shown that differences across major sulci across individuals are a matter of degree rather than a case of presence or absence (Connolly, 1950, External morphology of the primate brain, C.C. Thomas; Hecht et al., 2019 J Neurosci; Kawamuro 1971 Acta Anat., Kawamuro & Naito, 1977, Acta Anat.). In our revised manuscript, we aim to include some additional individuals of selected species as supplementary material, further illustrating this point.
We feel that measures such as sulci depth, sulci wall surface, or thickness of the cortical ribbon are measures that vary more across individuals and we have therefore not included them in the study. In addition, these are measures that are not generally used as between-species comparative measures, whereas sulcal patterning is (cf. Amiez et al., 2019, Nat Comms; Connolly, 1950; Miller et al., 2021, Brain Behav Evol; Radinsky 1975, J Mammal; Radinsky 1969, Ann N Y Acad Sci; Welker & Campos 1963 J. Comp Neurol).
Reviewer #2 (Public review):
Summary:
The authors have completed MRI-based descriptions of the sulcal anatomy of 18 carnivoran species that vary greatly in behaviour and ecology. In this descriptive study, different sulcal patterns are identified in relation to phylogeny and, to some extent, behaviour. The authors argue that the reported differences across families reflect behaviour and electrophysiology, but these correlations are not supported by any analyses.
Strengths:
A major strength of this paper is using very similar imaging methods across all specimens. Often papers like this rely on highly variable methods so that consistency reduces some of the variability that can arise due to methodology.
The descriptive anatomy was accurate and precise. I could readily follow exactly where on the cortical surface the authors referring. This is not always the case for descriptive anatomy papers, so I appreciated the efforts the authors took to make the results understandable for a broader audience.
I also greatly appreciate the authors making the images open access through their website.
Weaknesses:
Although I enjoyed many aspects of this manuscript, it is lacking in any quantitative analyses that would provide more insights into what these variations in sulcal anatomy might mean. The authors do discuss inter-clade differences in relation to behaviour and older electrophysiology papers by Welker, Campos, Johnson, and others, but it would be more biologically relevant to try to calculate surface areas or volumes of cortical fields defined by some of these sulci. For example, something like the endocast surface area measurements used by Sakai and colleagues would allow the authors to test for differences among clades, in relation to brain/body size, or behaviour. Quantitative measurements would also aid significantly in supporting some of the potential correlations hinted at in the Discussion.
Although quantitative measurements would be helpful, there are also some significant concerns in relation to the specimens themselves. First, almost all of these are captive individuals. We know that environmental differences can alter neocortical development and humans and nonhuman animals and domestication affects neocortical volume and morphology. Whether captive breeding affects neocortical anatomy might not be known, but it can affect other brain regions and overall brain size and could affect sulcal patterns. Second, despite using similar imaging methods across specimens, fixation varied markedly across specimens. Fixation is unlikely to affect the ability to recognize deep sulci, but variations in shrinkage could nevertheless affect overall brain size and morphology, including the ability to recognize shallow sulci. Third, the sample size = 1 for every species examined. In humans and nonhuman animals, sulcal patterns can vary significantly among individuals. In domestic dogs, it can even vary greatly across breeds. It, therefore, remains unclear to what extent the pattern observed in one individual can be generalized for a species, let alone an entire genus or family. The lack of accounting for inter-individual variability makes it difficult to make any firm conclusions regarding the functional relevance of sulcal patterns.
We thank the reviewer for their assessment of our work. The primary aim of this study was to establish a framework for navigating carnivoran brains by providing a comprehensive overview of all major neocortical sulci across eighteen different species. Given the inconsistent nomenclature in the literature and the lack of standardized criteria (“recipes”) for identifying the major sulci, we specifically focused on homogenizing the terminology and creating recipes for their identification. Moreover, we also generated digital surfaces of all brains and will also add sulcal masks to further facilitate future research building on our framework. We are pleased to hear that we succeeded in our primary objective.
We respectfully disagree with the reviewer on two accounts, where we believe the reviewer is not judging the scope of the current work.
The first is with respect to individual differences. To the best of our knowledge, differences between captive and wild animals, or indeed between individuals, do not affect the presence or absence of any major sulci. No differences in sulcal patterns were detected between captive and (semi-)wild macaques (cf. Sallet et al., 2011, Science; Testard et al., 2022, Sci Adv), different dog breeds (Hecht et al., 2019 J Neurosci) or foxes selectively bred to simulate domestication, compared to controls (Hecht et al., 2021 J. Neurosci). Indeed, we do not find major differences between wolf-like canid species, suggesting that a difference between individuals of the same species is even more unlikely. Nevertheless, we agree with the reviewer that building up a database like ours will benefit from providing as much information about the samples as possible to enable these issues to be tested. We, therefore, will update our table to include if the animals were from captive or wild populations. Moreover, we aim, where possible, to include both wild and captive animals of the same species if they are available in our revision.
The second is in the quantification of structure/function relationships. We believe the sulci atlases themselves are the main deliverables of this project. We felt it prudent to include some qualitative descriptions of the relationship between sulci as we observed them and behaviours as known from the literature as an illustration of the possibilities that this foundational work opens us. This approach also allowed us to confirm previous findings based on observations from a less diverse range of carnivoran species and families (Radinsky 1968 J Comp Neurol; Radinsky 1969, Ann N Y Acad Sci; Welker & Campos 1963 J Comp Neurol; Welker & Seidenstein, 1959 J Comp Neurol). However, a full statistical framework for analysis is beyond the scope of this paper. Our group has previously worked on methods to quantitatively compare brain organization across species — indeed, we have developed a full framework for doing so (Mars et al., 2021, Annu Rev Neurosci), based on the idea that brains that differ in size and morphology should be compared based on anatomical features in a common feature space. Previously, we have used white matter anatomy (Mars et al., 2018, eLife) and spatial transcriptomics (Beauchamp et al., 2021, eLife). The present work presents the foundation for this approach to be expanded to sulcal anatomy, but the full development of this approach will be the topic of future communications.
Nevertheless, we aim to include a first step quantitative analysis of the relationship between the presence and absence of particular sulci and the two behaviours of interest in our manuscript.
We also would like to emphasize that we strongly believe that looking at measures of brain organization at a more detailed level than brain size or relative brain size is informative. Indeed, studies looking at correlations between brain size and particular behavioural variables, although very prominent in the literature, have found it very difficult to distinguish between competing behavioural hypotheses (Healy, 2021, Adaptation and the brain, OUP). In contrast, connectivity has a much more direct relationship to behavioural differences across species (Bryant et al., 2024, bioRxiv), as does sulcal anatomy (Amiez et al., 2019, Nat Comms; Miller et al., 2021, Brain Behav Evol). Moreover, such measures are less sensitive to the effects of fixation since that will affect brain size but not the presence or absence of a sulcus.
Following the reviewer’s recommendations, we will endeavour to include an even broader range of species in the revised version.
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