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Feeding strategies and associated cognitive capacities among Plio-Pleistocene hominins: toward new perspectives using the ventromedial prefrontal cortex

Capacités cognitives associées aux stratégies de recherche de nourriture chez les hominines plio-pléistocènes : vers de nouvelles perspectives à partir du cortex préfrontal ventromédian
Margot Louail

Abstracts

Feeding and foraging behaviors can exert selective pressures among heterotrophic organisms that lead to morphological, physiological, and/or behavioral adaptations. Several studies showed that primates use complex cognitive abilities to adjust foraging strategies taking into account specific spatio-temporal context and already experienced events. Thus, it has been suggested that complex foraging strategies had a strong influence on the evolution of some cognitive abilities among primates, such as value-based decision-making. Following recent results showing that a cortical area, the ventromedial prefrontal cortex (VMPFC), is strongly associated with value-based decision-making, we previously explored the relationship between this region and ecological parameters (such as daily path length, mean group size, dietary quality) in extant primates. Among the five species studied (Macaca mulatta, M. fuscata, Gorilla gorilla, Pan troglodytes and Homo sapiens), those with broader diets and more complex foraging strategies exhibit a bigger VMPFC than species with a less diversified diet. We suggested that the capacity to switch foraging behaviors using memorized information may have been particularly favored among hominins of the Late Pliocene and especially Early Pleistocene, a period marked by several time intervals of increased climatic instability. Indeed, as these hominins faced critically changing environments, the ability to switch foraging behaviors and to fall back on alternative resources during periods of food scarcity probably played a strong influence on their diversity and evolution. This paper discusses the potential of a focus on the VMPFC to provide new insights into the evolution of foraging strategies and associated cognitive abilities (such as value-based decision-making) among hominins. As endocranial casts are the only available material to study brain anatomy on fossils, possible ways to measure this region from external cerebral markers are discussed.

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Editor’s notes

Received 20/01/2020, accepted after revisions 03/09/2020, published online 23/10/2020.

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1 Introduction

1Maintaining foraging efficiency can exert key selective pressures underlying natural selection in animals, leading to various physiological, morphological and/or behavioral adaptations (Altmann, 2006; MacArthur and Pianka, 1966). Among primates, several authors have suggested that ecological parameters associated with feeding strategies were the main drivers of the evolution of unusually large brains and cognitive complexity (e.g. DeCasien et al., 2017; González-Forero and Gardner, 2018; Milton, 1981, 1988). This hypothesis (‘Ecological Brain Hypothesis’; Milton, 1981, 1988) focuses on the cognitive demands associated with foraging, such as the representation of the complex and irregular distribution of food items in space and time, the use of extractive foraging strategies, the capacity to plan foraging strategies using memorized information from past events, as well as the capacity to switch behaviors in fluctuating environments (e.g. Milton, 1981, 1988; Rosati, 2017). Another hypothesis posits that the evolution of brain size and complexity within primates was mostly influenced by various aspects of sociality, such as living in large stable groups, maintaining group cohesion, and cooperative breeding (e.g. Dunbar, 1995, 1998; Dunbar and Shultz, 2007). Although social and ecological explanations are often treated as alternative hypotheses, it is more likely that both influenced the evolution of complex cognition and brain size (DeCasien et al., 2017; Rosati, 2017; van Schaik et al., 2012). Indeed, current lines of evidence support a mosaic pattern of brain evolution and cognition (Barton and Harvey, 2000; DeCasien and Higham, 2019; Hager et al., 2012), so it seems reasonable to consider that social and ecological parameters had different contributions on distinct brain structures and their associated cognitive capacities. Moreover, some social factors are not independent from ecological parameters. For example, groups tend to be larger in stable and productive environments or can be reduced due to feeding competition (Chapman and Chapman, 2000; van Schaik, 2016).

2Thus, understanding the ecological context in which a given cognitive function is mobilized is essential to help understand how distinct cognitive abilities, and their neural substrate, may have been favored to improve the efficiency with which a species deals with socio-ecological challenges. Thereby, investigating structural cerebral changes across various species can shed light on how environmental variations and ecological parameters exerted contrasting selection pressures on functionally different brain structures and associated cognitive capacities (Barks et al., 2015; Barton, 2000; Barton et al., 1995; DeCasien and Higham, 2019). Following these studies, our recent work explored how socio-ecological parameters explain the variation of distinct brain measurements among five extant primate species (Louail et al., 2019). In particular, we analyzed a precise cortical area, the ventromedial prefrontal cortex (VMPFC), associated with cognitive skills thought to be involved in decision making, behavioral flexibility and foraging strategies, such as the capacity to mentally represent and evaluate desired items in advance as a basis for the planning of future actions (Rosati, 2017; San-Galli et al., 2016). In line with these studies, our results suggest that VMPFC-associated cognitive capacities are enhanced among primates with complex feeding ecologies. A more developed VMPFC seems associated with an enhanced ability to adjust complex foraging strategies taking episodic memory into account. Moreover, we showed that the relationship between the VMPFC and dietary diversity is relatively specific as it is not captured using global cerebral measurements—the whole brain, for example—or a control region as the primary somatosensory cortex (S1) (Louail et al., 2019). This finding reinforces the idea that relationships between ecology, neurobiology and cognition can be better captured using cerebral areas involved in specific cognitive operations than the whole brain (e.g. Healy and Rowe, 2007; Logan et al., 2018).

3Considering this relationship between the VMPFC and feeding ecology in extant primates, we have suggested investigating its development among fossil primate species could help the comprehension of their past feeding ecologies and associated behavioral flexibility (Louail et al., 2019). Among hominins (modern humans, their direct ancestors and extinct relatives) who faced the increased climatic instability of the Late Pliocene and especially the Early Pleistocene (ca. 2.9 to 1 Ma), the capacity to adapt to novel or changing environmental conditions and dietary resources probably had a strong influence on their distinct evolutionary histories (e.g. Potts, 1998a, 1998b, 2013; Shultz et al., 2012). Most studies highlight the importance of dietary ecology and behavioral flexibility to explain the distinct evolutionary histories of Paranthropus and Homo (e.g. Wood and Strait, 2004). Notably, the increasing brain size and the complexification of cognition in Early Pleistocene Homo has been related to a more omnivorous diet and an enhanced adaptability to changing environmental conditions (e.g. Wood, 2009). However, past feeding ecologies of contemporary Paranthropus and Homo, and their capacities to face changing environments, are still debated (e.g. Lüdecke et al., 2018; Martin et al., 2020; Ungar et al., 2006; Ungar and Sponheimer, 2011; Wood and Strait, 2004). Thus, our previous work raises new questions: do size variations of the VMPFC among Plio-Pleistocene hominins reflect different feeding adaptations, and what are the possible ways to measure the VMPFC among fossils? This article provides a summary of our previous results, showing that dietary complexity is specifically and positively related with the size of the VMPFC. It discusses the potential of a focus on the VMPFC to provide new insights into foraging strategies and feeding adaptations of fossil hominins. Finally, as brains are not preserved through time and endocranial casts constitute the only available material to study fossil neuroanatomy, I discuss possible ways to measure this region from external cerebral markers.

2 The more diversified the diet, the bigger the VMPFC: enhanced value-based decision-making with complex feeding strategies among primates

4Efficient foraging in the wild necessitates optimizing the ratio between resources-associated costs and benefits. Food choice and foraging strategies are highly dependent on feeding preferences and available resources (Lambert and Rothman, 2015; Trapanese et al., 2019b; Züberbuhler and Janmaat, 2010), as well as the organism’s ability to find, transform and assimilate these resources. Numerous studies pointed out that it is unlikely that primates find enough resources to meet their energetic requirements relying only on fortuitous foraging. Rather, foraging should be directed towards specific resources. Primates have the capacity to use mental representations of where and when a specific dietary resource would be available and to plan the course of action necessary to obtain it, taking into account already experienced events (Janmaat et al., 2006a, 2006b, 2016; Noser and Byrne, 2007; Trapanese et al., 2019a; van Schaik, 2016). Therefore, they are thought to use complex cognitive abilities such as episodic memory, value-based decision-making and planning to determine their daily foraging path depending on a specific spatio-temporal context (Cunningham and Janson, 2007; Hayden et al., 2011; Rosati, 2017; Zuberbühler and Janmaat, 2010). Recent studies showed that a precise cortical area, the ventromedial prefrontal cortex (VMPFC, Figure 1), is strongly associated with decision-making and valuation based on episodic memory (Barron et al., 2013; Rushworth et al., 2012; San-Galli et al., 2016). Therefore, our previous study (Louail et al., 2019) focused on this region to better understand its relationship with socio-ecological factors among primates.

Figure 1

Figure 1

Delimitation of the VMPFC (in red) among primates and proposed geometric model as an elliptic cylinder encompassing left and right sides (blue dotted lines; a: mean width/2; b: mean height/2; c: maximum length). Left: coronal view, right: midsagittal view. Modified from Louail et al., 2019. CS: cingulate sulcus; MOS: medialorbital sulcus; RS: rostral sulcus; CC: corpus callosum; A: anterior, P: posterior, D: dorsal, V: ventral, M: mesial, L: lateral.

Délimitation du VMPFC (en rouge) chez les primates et modélisation géométrique proposée en tant que cylindre elliptique incluant les hémisphères gauche et droit (lignes bleues pointillées ; a : largeur moyenne/2 ; b : hauteur moyenne/2 ; c : longueur maximale). Vues coronale (à gauche) et mid-sagittale (à droite). Modifiée d’après Louail et al., 2019. CS : sillon cingulaire ; MOS : sillon medial-orbital ; RS : sillon rostral ; CC : corps calleux ; A: antérieur, P: postérieur, D: dorsal, V: ventral, M: mésial, L: latéral.

5Taking phylogeny into account, our previous results showed that the volume of the VMPFC (absolute volume and ratio VMPFC/brain) is strongly associated with ecological factors linked to foraging behavior, and notably dietary diversity; primate species with a more diversified diet exhibit a bigger VMPFC than species with a less diversified diet (Louail et al., 2019). In line with previous studies (Rosati, 2017; San-Galli et al., 2016), our results thus suggest that the capacity to select actions based on memorized information and according to a specific context may have been favored among primates that forage in complex and seasonal environments. Using more global cortical measurements (the whole brain volume, the gyrus rectus, or the primary somatosensory cortex S1) does not capture the relationship with dietary quality. Because it has been shown that some cognitive operations are specifically related to particular cortical areas and neural networks (e.g. Cabeza and Kingstone, 2006; Neubert et al., 2015), it is not surprising that this relationship is not observed when considering the whole brain size, the S1 cortex (not located in the frontal lobe and not thought to be implicated in executive functions) nor the gyrus rectus (which encompasses the VMPFC, but also subcallosal areas – more related to autonomic responses – as well as a part of the frontal pole, involved in more complex executive functions; see Louail et al., 2019 for references). We also focused on the ratio VMPFC/brain volumes, notably because it takes into account head size effects (e.g. Donahue et al. 2018; Semendeferi et al. 2002). We further observed that the relationship between the relative size of the VMPFC and dietary quality is even stronger than between the absolute volume of the VMPFC and dietary quality.

6Altogether, and in line with previous studies, our neuro-ecological approach emphasizes that precise brain regions – recognized as functionally important in a specific cognitive skill and in a precise ecological/behavioral context, and well described neuroanatomically – may better reflect the potential drivers of neuroanatomical diversity across primates than the whole brain (e.g. Healy and Rowe, 2007; Logan et al., 2018). These results thus suggest that the VMPFC may represent a reliable proxy to evaluate and discuss feeding paleo-ecologies, particularly dietary diversity, and behavioral flexibility among extinct primates, including fossil hominins. During the Early Pleistocene, some authors related the increased encephalization observed in the Homo lineage to the evolution of behavioral flexibility and adaptability to changing environmental conditions and dietary resources (Potts, 1998a, 1998b; Shultz et al., 2012; Ungar et al., 2006). For example, innovations in the use of habitat, space or resources – including the capacity to use, make tools and to develop a set of complex tool-related behaviors for food processing – probably increased the ability to switch foraging strategies in mosaic and seasonal environments (e.g. Lee, 1991; Ungar et al., 2006). Discussing the adaptations of cognitive abilities that occur in response to particular ecological conditions could greatly benefit from the analysis of precisely defined brain regions. Numerous studies have shown that, in various taxa such as fishes, birds, rodents, primates or insects, neuroanatomical variations between or within species can be related to ecological differences or differences in individuals’ lifestyle (e.g. Sherry et al., 1989; Barton et al. 1995; Scotto-Lomassese et al., 2000; Kozorovitskiy et al., 2005; Kihslinger and Nevitt, 2006; Campi and Krubitzer, 2010; Gonda et al., 2013). For example, the hippocampus, notably involved in spatial memory, was found to be larger in kangaroo rat species with multiple storage sites (Jacobs and Spencer, 1994), in gorilla species with larger home ranges (Barks et al., 2015) or even in human taxi drivers with extensive navigation experience (Maguire et al., 2000). Thus, exploring the development of the VMPFC among hominins could bring important insights into potential drivers of neuroanatomy and cognition among these taxa, and their feeding adaptations.

3 Investigating the development of the VMPFC among Plio-Pleistocene hominins: potential connections to foraging strategies and behavioral flexibility

7Environmental instability forces animals to deal with periods of food shortage. It may therefore act as an energetic constraint on brain development and metabolic activity, which is among the most metabolically expensive tissue (e.g. Mink et al., 1981), because developing and sustaining relatively large brains requires maintaining a consistent and sufficient energetic intake. This idea is generally referred as the ‘Expensive Brain Framework’ (Aiello and Wheeler, 1995; Isler and van Schaik, 2009; van Woerden et al., 2010). Several studies on extant animals showed that periods of food scarcity are indeed associated with reduction in overall brain size (e.g. Weisbecker et al., 2015; Luo et al., 2017; van Woerden et al., 2010, 2014). However, other studies have found that brain sizes are larger among catarrhine primates that exhibit less variability in their food intake than expected based on environmental seasonality (van Woerden et al. 2012, 2014); or among birds that migrate to variable and seasonal habitats (Sayol et al., 2016; Fristoe et al., 2017). These results are in line with the ‘Cognitive Buffer hypothesis’ (Allman et al., 1993; Deaner et al., 2003; Sol, 2009), which posits that environmental variability favored larger brains that provide cognitive abilities for behavioral flexibility. Yet, disentangling environmentally induced plastic responses and evolutionary adaptations as sources of neuroanatomical variations between populations or species is a crucial issue (Hall and Tropepe, 2020). Put differently: are neuroanatomical variations the results of evolutionary histories or of experiences during neurodevelopment? Due to brain phenotypic plasticity, changes within an individual’s lifetime can result in neuroanatomical changes (e.g. Lledo et al., 2006; D’Aniello et al., 2019). This may be particularly the case if changes occur during development, but it is well known that neurogenic processes continue to shape the brain beyond embryogenesis and childhood (see e.g. Eriksson et al., 1998; Gould et al., 1999; Kornack and Rakic, 1999 for adult neurogenesis in primates, including humans). In our case, we make no claim at the possibility to disentangle these sources of neuroanatomical variations among extinct hominins, notably due to the temporal scale that can be considered. Moreover, it seems reasonable to assume that both sources of variations impacted hominin neuroanatomy: among other potential factors, increased environmental variability during Plio-Pleistocene might have induced an increase in brain plasticity and behavioral flexibility within an individual’s lifetime, and environmental variability over long time periods might have favored these individuals with an enhanced behavioral flexibility.

8During the Late Pliocene and the Early Pleistocene, faunal assemblages and paleoclimatic records suggest shifts toward increasingly variable and drier climatic conditions in Africa, with a global trend toward increased seasonality and more open environments (deMenocal, 2004). Even more than the tendency to aridification, the increasing alternance, and amplified differences, between hot/wet and cold/dry periods – from 2.9 Ma, and even more after 1.8 Ma – likely played a key role in the evolution of faunal lineages, including hominins (deMenocal, 2004; Potts, 1998a, 1998b, 2013). From ca. 2.9 to 1 Ma, hominin evolution was marked by key evolutionary events including speciation and lineage extinction, a high diversity of species, and significant changes in species morphology, such as an increasing variability in cranial capacity in Homo from 1.8 Ma (Prat, 2018). It is commonly agreed that the Australopithecus genus became extinct (last known species Au. sediba at 1.97 Ma; Pickering et al., 2011) and that two hominin lineages emerged during this time interval: the robust genus Paranthropus (first occurrence at 2.7 Ma; Constantino and Wood, 2004), including two to three commonly accepted species (P. aethiopicus and P.boisei in East Africa, and P. robustus in South Africa), and the more gracile genus Homo (first occurrence at 2.8 Ma; Villmoare et al., 2015). It is mostly accepted that Paranthropus became extinct ca. 1 Ma (Constantino and Wood, 2004) whereas Homo succeeded and expanded. Different feeding ecologies may explain the diversity within Plio-Pleistocene hominins and their evolutionary histories, notably between contemporary Paranthropus and Homo. Early Homo, with their small cheek teeth compared to other hominins, have long been considered to have an omnivorous diet (e.g. Wood, 1992; Wood and Collard, 1999). A broader range of dietary resources, including an increased amount of animal matter, along with technical innovations that could have helped to forage or process food items (such as the use and making of tools for processing foods, extracting bone marrow, foraging embedded foods), could explain the increasing brain size and the increasing complexity of cognitive abilities (e.g. Aiello and Wheeler, 1995; Wood, 2009). In contrast, Paranthropus, because of their robust masticatory system, was suggested to have a strictly vegetarian diet specialized in hard foods (Peters, 1987; Robinson, 1963). Their large and robust jaws and cheek teeth are thought to be well suited to process and consume mechanically challenging foods (Hylander, 1988). However, a large number of studies, based notably on enamel isotopic compositions and microwear analyses, showed a more diversified diet in Paranthropus, and argued that Paranthropus and early Homo were both likely to be ecological generalists and have a high behavioral flexibility (Lüdecke et al., 2018; Sponheimer et al., 2006; Ungar and Sponheimer, 2011; Wood and Strait, 2004). Moreover, numerous studies suggest different feeding ecologies between South and East African Paranthropus species, as well as important variability within species (e.g. Martin et al., 2020; Ungar and Sponheimer, 2011). Feeding ecologies of Plio-Pleistocene hominins and their associated behavioral flexibility and ecological niches are still a matter of debate.

9Several studies have suggested that critical environmental changes during the Late Pliocene and the Early Pleistocene put strong selective pressures on the cortical organization of early hominins and their associated cognitive abilities (e.g. Beaudet et al., 2019; Melin et al., 2014; Potts, 1998a, 1998b, 2004). Although we do not pretend to infer a causal link between environmental changes and cortical organization, we hypothesize that observed differences between hominins over time, or even between species, regarding the development of the VMPFC could be related to periods of strong environmental shifts. Indeed, these climatic events probably induced important changes in their ecological niches, and consequently in their feeding strategies and their behavioral flexibility. As explained above, dealing with food source uncertainty is both energetically expensive and cognitively challenging. The ability to switch to alternative food resources requires a capacity to store, recall and integrate information from past experiences as a basis for foraging decisions. Moreover, the foraging and processing of challenging foods – such as embedded food or underground storage organs (nuts, invertebrates, tubers), which are covered with protective matrices or hidden – might lead to anatomical (mainly on the masticatory system) and/or behavioral adaptations among hominins (Marshall and Wrangham, 2007). For example, the use and making of tools to slice meat and pounding underground storage organs (Zink and Lieberman, 2016). In line with these studies, exploring the development of the VMPFC among Late Pliocene and especially Early Pleistocene hominins may provide novel and complementary information to infer their past feeding ecologies and to discuss their behavioral flexibility. Differences in the size of the VMPFC may suggest differences in feeding ecologies and associated cognitive skills through time and/or between or within genera and species. If so, could changes in the development of the VMPFC be related to strong periods of environmental instability and changing available resources? Moreover, several lines of evidence suggest that hominins exploited a diversity of habitats and dietary resources, with inter and intra-specific differences over time and between African localities (e.g. Martin et al., 2020; Wood and Strait, 2004). Investigating the development of the VMPFC among these taxa could contribute to those discussions.

4 Preliminary insights into the estimation of the volume of the VMPFC from external cerebral markers

10Before attempting to investigate its size variations among fossil species, a crucial preliminary step is to identify potential means to delimit the VMPFC on cranial endocasts. Indeed, as brain tissues are not preserved through time, natural endocranial casts and virtual endocranial surfaces constitute the only available sources of information to infer brain characteristics in extinct primates, and thus to interpret hominin brain evolution. These casts are replicas of the inner surface of the braincase and, therefore, cannot provide information about subcortical structures, but they do reproduce some details of the external cerebral morphology (e.g. Beaudet and Gilissen, 2018). To examine and interpret fossil endocranial characteristics, paleoneurologists primarily rely on comparative neuroanatomy from extant species, and use atlases and cortical maps (Albessard-Ball and Balzeau, 2018; Beaudet et al., 2019; Bruner et al., 2017; Carlson et al., 2011; Falk, 1981, 2014; Falk et al., 2018; Holloway et al., 2004). They mostly rely on the presence/absence of the imprinted convolutions, their position or shape, as well as global dimensions of cerebral lobes. Few studies on fossil hominins have focused on more precise regions than cerebral lobes, associated with cerebral areas that were defined on the basis of functional and/or cytoarchitectonic (ie. cellular composition) characteristics (e.g. Holloway et al., 2018; Balzeau et al. 2014; Carlson et al., 2011; Falk et al., 2009; see also Falk, 2014 for implications of comparative cytoarchitectonic studies for interpreting macroscopic morphology on hominin endocasts). The limited number of cerebral traits on endocranial surfaces and the weak correspondence between sulcal landmarks and cytoarchitectonic areas are challenges for this type of work.

11Cortical areas, frequently referred to as Brodmann’s areas, are largely defined on the basis of differences in their cellular composition (cytoarchitectonics) and on connectivity maps. Numerous studies have shown that sulci and borders of cytoarchitectonic areas do not coincide (Brodmann, 1909; Vogt and Vogt, 1919), or only coincide in a few examples (Roland et al., 1997; Zilles et al., 1997). Consequently, some authors argued that sulcal landmarks were not reliable proxies of the microstructural organization of the cortex and that microscopic features should instead be considered. As a consequence, considerable efforts have been made, despite substantial anatomical variability between individuals, to bridge the gap between functional, cytoarchitectonic and structure-based mapping in order to integrate functional and structural data in a common anatomical reference (see e.g. Amunts and Zilles, 2015 for a review). Although it is commonly agreed that sulci do not correlate precisely with the borders of cerebral areas, recent works have shown that cortical folding patterns correspond more to borders of some cytoarchitectonic areas than previously thought (e.g. Fischl et al., 2008; Weiner and Zilles, 2016). As defined in our previous study (Louail et al., 2019), the VMPFC strongly overlaps with Brodmann area 14r. Aiming to extend the analysis of this region to extinct species, we used macroscopic landmarks to delimit it through different primate species, and our results match the observations of functional studies. Thus, it seems reasonable to use some of these macroscopic features to target this area on cranial endocasts.

12The VMPFC is located on the ventral surface of the prefrontal cortex, between the left and right medialorbital sulci (MOS; Figure 1). Some of its borders are subcortical structures. Its anterior and posterior limits correspond, respectively, to the most anterior part of the (para)cingulate sulcus and to the genu of the corpus callosum. Its upper limit corresponds to the fundus of the rostral sulcus. Hence, these limitations challenge the possibility to reliably estimate the dimensions of the VMPFC on different primate species. We do not make any assumptions regarding the possibility to localize these borders. However, its position on the ventral surface suggests it may be observable on cranial endocasts, conversely to cortical areas located on the medial surface of cerebral hemispheres for example. Among the landmarks used, medialorbital sulci correspond approximately to the lateral borders of the area. These sulci are located on the ventral surface of the orbitofrontal cortex. Thus, it seems reasonable to assume that they could be useful to locate this specific area on cranial endocasts. Moreover, a recent study showed that the MOS is identifiable on the endocasts of 8 of the 10 primate species studied (Kobayashi et al., 2018). Although the exact localization of the lateral border – the folding of the cortex – is determined using the morphology of the cortical gray matter, the VMPFC should be targetable between these sulci. Indeed, as the VMPFC is located on the most medial part of the orbitofrontal cortex, this is the only area visible on the middle of the ventral surface between these two sulci. As such, a surface estimation between these boundaries could provide some insights into the development of this cortical area among fossil species, even if this measurement does not allow us to fully capture the specific relationship with feeding ecology. However, Balzeau et al. (2012) showed that variations in the surface of lobes measured on endocasts contradict variations of the volume. Thus, these authors argued that variations in surface are not “a good indicator of their variations in total size or volume”. Consequently, an analysis of the surface variations of the VMPFC on extant primates could be conducted to assess whether these surface measurements also capture a relationship with feeding ecology, notably dietary diversity.

Figure 2

Figure 2

Estimation of the VMPFC as an elliptic cylinder with dimensions shown in Fig. 1 (a: mean width/2; b: mean height/2; c: maximum length) and corresponding volume formula.

Modélisation géométrique du VMPFC en tant que cylindre elliptique avec les dimensions a, b et c présentées sur la Figure 1 (a : largeur moyenne/2 ; b : hauteur moyenne/2 ; c : longueur maximale) et sa formule mathématique pour calculer son volume.

13Our previous results showed a relationship between feeding ecology and the volume of the VMPFC (Louail et al., 2019), but we did not investigate if this relationship is captured with surface measurements. Since we attempt to infer some aspects the feeding paleo-ecologies of fossil hominins, some ideas are considered for a volume estimation overcoming the lack of medial landmarks, given the impossibility of measuring the precise gray matter volume. Although I suggest using information from endocranial surfaces to infer volume variations, I do not propose only considering surface variations as an indicator of volume variations. A geometric model with a known formula to measure its volume, such as a cylinder, could help estimate the development of the VMPFC. It thus avoids the quantification of the precise gray matter amount within the VMPFC, and the necessity to localize all of its boundaries. In view of its global morphology (Figure 1), the VMPFC might be considered an elliptic cylinder (Figures 1 and 2), with its respective formula to estimate its volume. However, this model requires determining the length of the VMPFC (c), its width (2a) and its height (2b) to measure its volume. Consequently, although it seems to be a grosser geometric model than the elliptic one, a simple cylinder should also be considered, as it only requires knowing, for example, the length and the width. Taking these limitations altogether, can a volume approximation of the VMPFC using external cerebral markers on brain endocasts still capture its specific relationships with feeding ecology through primate species? This method could be used to test if it introduces some variability that may not have any biological meaning, or if this variability can be related to feeding ecology, as shown with the measured volume of the VMPFC on brain tissues. At last, our previous results on the ratio VMPFC/brain showed an even stronger relationship with dietary quality (accounting for 40% of the total variance observed). This relative measurement reduces the effects only related to individual variations in brain size, or related to sex or age (although we did not observe significant differences between sexes or ages). Among fossils, this relative measurement should also be considered to reduce the effects only linked to individual variations in brain size, age or sex, particularly considering that some taxa may exhibit more sexual dimorphism than others. Moreover, as endocranial volume is somewhat larger than brain volume, considering this relative measurement could take into account endocranial volume variations not substantially related to brain volume variations. These ideas should be followed and examined in further research aiming to explore the development of the VMPFC among fossil primates.

Acknowledgments

14I thank the Francophone Society of Primatology for having supported this research project. I thank Sebastien Bouret, Cecile Garcia and Sandrine Prat for the supervision of this project and their careful review of the manuscript, as well as Emmanuel Gilissen for his very valuable contribution to this work. I thank Lou Albessard-Ball and Alice Louail for their careful review of the manuscript and English corrections. I received the ‘Tremplin’ grant of the Francophone Society of Primatology for this research project. This work was also supported by the Programme Emergence (PrimEvoCog SU-16-R-EMR-09-01) from Sorbonne Universités, Idex SUPER (Paris, France) (to S. Bouret, C. Garcia and S. Prat) and the ANR project HOMTECH (ANR-17-CE27-0005) (to S. Prat). I also thank the reviewers, Antoine Balzeau and an anonymous one, whose comments greatly improved the manuscript.

Competing interests

15The author declares there is no potential conflict of interest.

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List of illustrations

Title Figure 1
Caption Delimitation of the VMPFC (in red) among primates and proposed geometric model as an elliptic cylinder encompassing left and right sides (blue dotted lines; a: mean width/2; b: mean height/2; c: maximum length). Left: coronal view, right: midsagittal view. Modified from Louail et al., 2019. CS: cingulate sulcus; MOS: medialorbital sulcus; RS: rostral sulcus; CC: corpus callosum; A: anterior, P: posterior, D: dorsal, V: ventral, M: mesial, L: lateral.
URL http://journals.openedition.org/primatologie/docannexe/image/7157/img-1.png
File image/png, 167k
Title Figure 2
Caption Estimation of the VMPFC as an elliptic cylinder with dimensions shown in Fig. 1 (a: mean width/2; b: mean height/2; c: maximum length) and corresponding volume formula.
URL http://journals.openedition.org/primatologie/docannexe/image/7157/img-2.png
File image/png, 36k
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References

Electronic reference

Margot Louail, Feeding strategies and associated cognitive capacities among Plio-Pleistocene hominins: toward new perspectives using the ventromedial prefrontal cortexRevue de primatologie [Online], 11 | 2020, Online since 23 October 2020, connection on 24 June 2025. URL: http://journals.openedition.org/primatologie/7157; DOI: https://doi.org/10.4000/primatologie.7157

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About the author

Margot Louail

UMR 7225 - INSERM U1127 - UPMC UMR S 1127, Hôpital Pitié-Salpêtrière, 47 Boulevard de l'Hôpital, 75013 Paris, France (2) UMR 7194 (HNHP), MNHN/CNRS/UPVD, Association Sorbonne Université, Musée de l’Homme, 17 Place du Trocadéro, 75116 Paris, France, louailmargot@gmail.com

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The text only may be used under licence CC BY-NC-ND 4.0. All other elements (illustrations, imported files) are “All rights reserved”, unless otherwise stated.

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