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# The diploic venous system in *Homo neanderthalensis* and fossil *Homo sapiens*: A study using high-resolution computed tomography

Jiaming Hui, Antoine Balzeau

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## To cite this version:

Jiaming Hui, Antoine Balzeau. The diploic venous system in *Homo neanderthalensis* and fossil *Homo sapiens*: A study using high-resolution computed tomography. American Journal of Biological Anthropology, 2023, 182 (3), pp.412 - 427. 10.1002/ajpa.24843. hal-04250485

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Submitted on 19 Oct 2023

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# The diploic venous system in *Homo neanderthalensis* and fossil *Homo sapiens*: A study using high-resolution computed tomography

Jiaming Hui<fnref n="1" />,<fnref n="2" /> ID | Antoine Balzeau<fnref n="1" />,<fnref n="3" />

## Correspondence

Jiaming Hui, UMR 7194 Histoire Naturelle de l'Homme Préhistorique, Muséum national d'Histoire naturelle, 17 place du Trocadéro, Paris, 75016, France.

Email: jiaming.hui@etu.sorbonne-universite.fr

## Funding information

Agence Nationale de la Recherche, Grant/Award Number: ANR-20-CE27-0009; China Scholarship Council

## Abstract

**Objectives:** The diploic venous system has been hypothesized to be related to human brain evolution, though its evolutionary trajectory and physiological functions remain largely unclear. This study examines the characteristics of the diploic venous channels (DCs) in a selection of well-preserved *Homo neanderthalensis* and Upper Paleolithic *Homo sapiens* crania, searching for the differences between the two taxa and exploring the associations between brain anatomy and DCs.

**Materials and Methods:** Five *H. neanderthalensis* and four *H. sapiens* fossil specimens from Western Europe were analyzed. Based on Micro-CT scanning and 3D reconstruction, the distribution pattern and draining orifices of the DCs were inspected qualitatively. The size of the DCs was quantified by volume calculation, and the degree of complexity was quantified by fractal analyses.

**Results:** High-resolution data show the details of the DC structures not documented in previous studies. *H. neanderthalensis* and *H. sapiens* specimens share substantial similarities in the DCs. The noticeable differences between the two samples manifest in the connecting points surrounding the frontal sinuses, parietal foramina, and asteroidal area.

**Discussion:** This study provides a better understanding of the anatomy of the DCs in *H. neanderthalensis* and *H. sapiens*. The connection patterns of the DCs have potential utility in distinguishing between the two taxa and in the phylogenetic and taxonomic discussion of the Neandertal-like specimens with controversial taxonomic status.

## KEYWORDS

brain evolution, craniovascular system, fossil hominins, micro-CT

## Research Highlights

* Micro-CT reveals the undiscovered draining orifices in fossils.

* *H. sapiens* specimens do not display more developed diploic venous networks compared with *H. neanderthalensis* sample.

* The diploic veins have potential utility in taxonomic analyses.

**Abbreviations:** AMV, anterior meningeal vessel; CS, cavernous sinus; DC, diploic channel; EV, emissary vein; FS, frontal sinus; MMV, middle meningeal vessel; PF, parietal foramen; PMV, posterior meningeal vessel; PSQS, petrosquamous sinus; SPHS, sphenoparietal sinus; SPS, superior petrosal sinus; SSS, superior sagittal sinus; TSS, transverse sinus and sigmoid sinus.

This is an open access article under the terms of the [Creative Commons Attribution License](https://creativecommons.org/licenses/by/4.0/), which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

© 2023 The Authors. *American Journal of Biological Anthropology* published by Wiley Periodicals LLC.

<footnote n="1">¹PaleoFED team, UMR 7194 Histoire Naturelle de l'Homme Préhistorique, CNRS, Département Homme et Environnement, Muséum national d'Histoire naturelle, Paris, France</footnote>

<footnote n="2">²Ecole Doctorale 227 Sciences de la nature et de l'Homme : évolution et écologie, Sorbonne Université, Paris, France</footnote>

<footnote n="3">³Department of African Zoology, Royal Museum for Central Africa, Tervuren, Belgium</footnote>
# 1 | INTRODUCTION

The cranial vascular system is integral to brain evolution, as it maintains the metabolic process of the brain and protection layers (Aiello & Dean, 1990; Lieberman, 2011; Píšová et al., 2017). While much evidence reveals the evolutionary trajectory of the dural sinuses and meningeal vessels (Bruner et al., 2006, 2011; Falk, 1986; Falk & Conroy, 1983; Saban, 1995), another essential component of the cranial vascular network—the diploic veins—is rarely explored in fossil hominins, despite two pioneering studies testing the procedures for visualizing the diploic vessels in *Homo sapiens*, *Homo neanderthalensis*, and *Homo rhodesiensis* (Rangel de Lázaro et al., 2016, 2018).

Studies on living people and cadavers show that the diploic veins are valveless vessels transporting venous blood and cerebrospinal fluid (García-González et al., 2009; Lachkar et al., 2019; Tsutsumi et al., 2014, 2015; Yamashiro et al., 2021). They are connected with the extra-cranial veins, meningeal vessels, and dural sinuses. The diploic venous network is variable and it can be described as “developed” if it possesses large lumen sizes, long branch lengths, many anastomoses, and many ramifications (Hershkovitz et al., 1999; Rangel de Lázaro et al., 2020). These characteristics can improve its ability in transporting blood (Jain, 1988; Schmidt & Thews, 1989). The diploic vessels are embedded in the diploic channels (DCs), the bony tubes running in the diploic layer, between the inner and outer tables of the calvarial bones. The enclosed space can protect the DCs from taphonomic processes, and thus it allows us to reconstruct the diploic venous networks in extinct hominin species. On the other hand, the hard cranial bones covering the DCs lead to difficulties in dissection. In addition, the small diameters of some DC branches make traditional visual inspections difficult. For these reasons, observing the DCs is an enduring challenge in anatomy and anthropology (García-González et al., 2009; Píšová et al., 2017), which explains the limited number of such studies in fossil hominins.

Differences across many hominin species have been identified in the meningeal vessels and dural sinuses (Bruner et al., 2006, 2011; Falk, 1986; Falk & Conroy, 1983; Saban, 1995). Especially, in the comparison between *H. neanderthalensis* and *H. sapiens*, studies highlight that the former has less complex MMVs, a higher incidence of PSQS, and a greater deviation between SSS and midline (Balzeau & Pagano, 2022; Bruner et al., 2006; Peña-Melián et al., 2011; Píšová et al., 2017; Rosas et al., 2014). As the DC network is a system highly integrated with these meningeal vessels and dural sinuses, the DCs may have morphological changes together with these vascular networks. Thus, it is reasonable to expect the DCs to show differences between species. However, few anatomical studies compared the morphology of the DCs across different taxa.

With projectional radiography and clinical CT scanner, few studies have discussed the phylogenetic and taxonomic implications of the DCs. Hershkovitz et al. (1999) compare the DC systems between extant humans and nonhuman primates, suggesting that humans have more reticulated DC branches, but the limited sample size of nonhuman primates cannot guarantee the reliability of these results. Rangel de Lázaro et al. (2016) compare three *H. neanderthalensis* fossil

specimens with the dry crania of extant humans, arguing that the latter has more complex DCs. Still, the CT slice thicknesses of *H. neanderthalensis* specimens (0.46–1.00 mm) in their study may be higher than the diameters of some DC branches, which range from 0.5 to 4.2 mm in extant adult humans (Rangel de Lázaro et al., 2016). This may lead to difficulties in visualizing some parts of the DC network. In other words, the taxonomic signal and the potential for phylogenetic applications should be tested with more empirical data.

The role of the DCs in brain evolution also remains unclear. In paleoneurology, there is an ongoing debate on the possible associations between brain morphology and cranial vascular networks. For instance, it has been questioned whether the complexity of the meningeal vessels is related to encephalization (Bruner et al., 2006, 2011; Saban, 1995). Similarly, in the last few decades, the association with the brain has been a central issue in the studies on the DCs (Hershkovitz et al., 1999; Píšová et al., 2017; Rangel de Lázaro et al., 2016, 2020). In the frequently discussed “radiator theory,” it is hypothesized that the DCs with other veins extending intra-cranially may condition the increase of brain volume, as an oversized brain may generate heat loads exceeding the thermoregulatory capability of these vessels and leading to tissue damage (Cabanac & Brinnel, 1985; Falk, 1990; Kunz & Iliadis, 2007; Lieberman, 2011; White et al., 2011). Thus, the DC network may be related to the evolution of endocranial capacity, with larger brains hypothesized to have more developed DC networks than smaller brains (Kunz & Iliadis, 2007). However, the “radiator theory” can be challenged since it did not rely on the observation of the internal structures in fossils. Therefore, the theory has no direct evidence from morphology estimating whether the evolution trend of the DCs, if there is any, is related to the progressively changing brain size.

In this regard, a comparison between *H. neanderthalensis* and *H. sapiens* will be of significance. In particular, as the two groups have similar endocranial capacities (Aiello & Dean, 1990; Bruner et al., 2003; Schwartz et al., 2002), it allows us to estimate whether they have comparably developed DCs as hypothesized. This is especially interesting because the current understanding is that some *H. neanderthalensis* specimens (Saccopastore 1, Spy 1, and Spy 10) seem to have less developed DC networks than extant humans (Rangel de Lázaro et al., 2016). What is more, the preservation of fossils should also be considered. As a large amount of *H. neanderthalensis* crania have well-preserved diploë, this makes comparative anatomical studies possible.

In general, to provide further insights into the significance of the diploic venous system in human evolution, we need to include more fossils in anatomical studies with higher-resolution imaging methods to reconstruct entire DC networks. Here, with Micro-CT imaging able to detect the small-diameter DCs, this study aims to (1) examine the characteristics of the DCs in a selection of well-preserved *H. neanderthalensis* and Upper Paleolithic *H. sapiens* fossils in order to discuss their potential similarities and differences, and to (2) explore the possible association between the morphology of the DCs and brain evolution.
# 2 | MATERIALS AND METHODS

## 2.1 | Materials

The study included five crania attributed to *H. neanderthalensis* and four crania attributed to *H. sapiens* (Table 1). The *H. neanderthalensis* specimens were the so-called “Classic Neanderthals,” with most of the specimens dated to 54–40 ka (MIS 3), and the Upper Paleolithic *H. sapiens* specimens were dated to 28–26 ka (MIS 2). The specimens selected were overall well preserved and the diploic structures were observable. To avoid any variation related to ontogenetic processes (Hershkovitz et al., 1999; Rangel de Lázaro et al., 2020), we only selected adult specimens.

## 2.2 | Reconstruction of 3D models

Visualizing an entire DC network was difficult for clinical CT scanners, for their slice thicknesses were usually above 1 mm (Ford & Decker, 2016; Guggenbuhl et al., 2008; Treece et al., 2010), which was higher than the diameters of some DC branches (García-González et al., 2009; Rangel de Lázaro et al., 2020). To improve the reconstruction of the DC network, we used the Micro-CT images with slice thicknesses set below 0.15 mm (Table 1). Spy 1 and Spy 10 were imaged by the scanner “RX Solutions EasyTom 150,” and the other specimens were with the scanner “Phoenix V|tome|x L240.” The internal structures wider than 0.3 mm could be displayed clearly in Micro-CT images, which enabled us to detect narrow DCs and draining orifices (Figure S1). The Micro-CT image stacks were processed in ImageJ v1.53t (Schneider et al., 2012) by adjusting the window width and window level to clearly define the boundaries of the DCs. Then, by converting the images from 16-bit to 8-bit, we reduced the data size by 50%. It accelerated the following processes by compromising the display of intensity variation of bone tissues. However, it did not affect our analyses, as we focused on the cavities rather than on the intensity of bones.

To locate the DCs (Figure 1), we then reconstructed the 3D cranial models in 3D Slicer v4.13 (Fedorov et al., 2012). More specifically, the “Threshold” and “Paint” functions semi-automatically segmented the bone tissues, including the tables and diploic cancellous bones, but excluding the diploic cavities. 3D Slicer automatically displayed the 3D model of these bone tissues based on the segmentation. In this way, the 3D model duplicated the surface of a real cranium and its internal diploic structures. Thus, the 3D model also contained diploic cavities, which were visible after setting an opacity level of 50%. In the diploic layer, some cavities were DCs, while the others might be containers of marrow or air (Balzeau & Radovčić, 2008; Francies et al., 2017; Loevner et al., 2002; Som & Lawson, 2008). The criteria we used to identify a diploic cavity as a DC were: (1) the cavity should be in the shape of a vessel, and (2) it should have anastomosis with the extra-/intra-cranial vascular network or other DCs. The junc- ture where a DC connected to a non-vessel-like structure was consid- ered the end of this DC branch. DC main branches and most small branches could be recognized from the 3D view of the transparent cranial model. Some small branches were difficult to recognize in this way for their sheltered locations, which required us to inspect the 2D cross sections of these branches.

After recognizing the DCs, we constructed their 3D models with the “Flood filling” function in 3D Slicer (Figure 1). The mechanism was that, after manually marking one voxel of a DC branch as the starting point, the algorithm could automatically segment all the voxels con- nected to and with similar intensity levels (i.e., gray levels) to the start- ing point. “Flood filling” also allowed us to set the “intensity tolerance level” (i.e., threshold of similarity). If the difference in intensity between a voxel (e.g., bone voxel) and the starting point was over the threshold, the voxel would be excluded automatically. The voxels of a DC branch usually shared similar intensity levels, which were close to those of air and much lower than those of bone tissues, because the DCs were usually empty. As the intensity levels of DCs and bones were variable, we adjusted the intensity tolerance level according to the situation in each location, but it usually stood at 10 gray levels. In most cases, this intensity tolerance level allowed “Flood filling” to

<table><caption>TABLE 1 The inventory of the fossils.</caption><thead><tr><th></th><th>Name</th><th>Material source</th><th>Micro-CT voxel size (mm)</th><th>Marine isotope stages</th><th>Reference</th></tr></thead><tbody><tr><td rowspan="5">Homo neanderthalensis</td><td>La Chapelle-aux-Saints 1</td><td>MH</td><td>0.123</td><td>MIS 3?</td><td>(Raynal & Pautrat, 1990)</td></tr><tr><td>La Ferrassie 1</td><td>MH</td><td>0.132</td><td>MIS 3?</td><td>(Guérin et al., 2015)</td></tr><tr><td>La Quina H5</td><td>MH</td><td>0.109</td><td>MIS 4?</td><td>(Verna, 2006)</td></tr><tr><td>Spy 1</td><td>RBINS</td><td>0.095</td><td>MIS 3</td><td>(Devièse et al., 2021)</td></tr><tr><td>Spy 10</td><td>RBINS</td><td>0.096</td><td>MIS 3</td><td>(Devièse et al., 2021)</td></tr><tr><td rowspan="4">Homo sapiens</td><td>Abri Pataud</td><td>MH</td><td>0.110</td><td>MIS 2</td><td>(Douka et al., 2020)</td></tr><tr><td>Cro-Magnon 1</td><td>MH</td><td>0.115</td><td>MIS 2</td><td>(Henry-Gambier, 2002)</td></tr><tr><td>Cro-Magnon 2</td><td>MH</td><td>0.110</td><td>MIS 2</td><td>(Henry-Gambier, 2002)</td></tr><tr><td>Cro-Magnon 3</td><td>MH</td><td>0.110</td><td>MIS 2</td><td>(Henry-Gambier, 2002)</td></tr></tbody></table>

Note: MIS = Marine isotope stage; MH = Musée de l'Homme, Paris, France; RBINS = Royal Belgian Institute of Natural Sciences, Brussels, Belgium. The fossil Spy 10 was sometimes referred to as Spy 2 in previous fossil records.
<figure><img src="image_4.png" /><figcaption>**FIGURE 1** The workflow of segmentation. Based on CT images (a), the “Threshold” and “Paint” functions in 3D Slicer semi-automatically segment all bone tissues (b, yellow) and leave the diploic cavities (b, scattered dark holes inside the yellow segment). 3D Slicer automatically constructs the 3D cranial model of segment (c), which duplicates the diploic structures of the real cranium. By setting the opacity level and zooming in (d), we can recognize the DCs from the 3D and 2D views (e, blue arrows). Finally, with the “Flood filling” and “Paint” functions, we segment the DCs and construct their 3D model (f, blue segment).</figcaption></figure>

segment all the voxels of a DC branch and to exclude the bones. Thus, after setting the intensity tolerance threshold and manually selecting one voxel of one DC branch as the starting point, “Flood filling” could automatically segment this branch and leave the bone tissues (Figure 2). By applying this process to every DC branch separately, we could gradually construct the 3D model of an entire DC network.

Still, some DC branches displayed intensity levels very close to bone tissues. “Flood filling” was not applicable to this situation, and we instead segmented their voxels manually with the “Paint” function. Occasionally, the segments made by “Flood filling” included some structures generated by taphonomic processes. We used the “Eraser” function to erase the connections between these taphonomic structures and DC branches, and then we used the “Island” function to

remove the taphonomic structures. The mechanism of the latter function was that, by marking one voxel, the function could automatically remove all its connected segments.

## 2.3 | Qualitative and quantitative analyses

The distribution of the DCs was inspected qualitatively. Especially, for the parietal bone, the area with highly variable distribution patterns (García-González et al., 2009; Hershkovitz et al., 1999), we used the categorization method established by Hershkovitz et al. (1999). The method classified the parietal DCs into seven patterns: spider, serpentine, coronal, bonsai, thousand lakes, hybrid, and indeterminate
<figure><img src="image_5.png" /><figcaption>**FIGURE 2** The workflow shows how to pre-process a DC pattern before fractal analyses. Orthographic screenshots of every small section with overlapping fields are taken from a 3D model (a). They are then stitched together to form a 2D pattern (b) and finally converted into a binary image (c).</figcaption></figure>

(Figure S3). In addition, to inspect the connection pattern of the DCs, we traced their pathways and detected the orifices. This could show us how the DCs anastomose with the frontal sinuses, dural sinuses, meningeal vessels, emissary vessels, and extra-cranial veins.

The size and complexity of a vessel reflect its ability in transporting blood. A large size means the vascular system may contain and deliver a large amount of blood (Jain, 1988; Schmidt & Thews, 1989). A high degree of complexity means the vascular system may have many ramifications and anastomoses, which can deliver the blood to more areas and provide collateral pathways for blood drainage (Coyle & Heistad, 1991; Jain, 1988; Schmidt & Thews, 1989). Compared with a less developed DC network, a highly developed network should simultaneously possess a bigger size and a more complex branching pattern (Hershkovitz et al., 1999; Rangel de Lázaro et al., 2020). In this study, the size of the DCs was quantified by volume calculation, and the degree of complexity was quantified by fractal analyses.

Considering that the absolute DC volume of incomplete fossils might not represent the real size of the DC networks, this study introduced the DC volume index, whose formula was: DC volume index = (DC volume/Bone tissue volume) × 100. The bone tissue volume referred to the volume of cranial tables and diploic cancellous bones, excluding the diploic cavities. The index not only helped us correct the problem of preservation, but also showed us the relative size of the DCs inside a bone. Before the calculation, we inspected 3D cranial models and CT images to locate the areas affected by taphonomic damages that might distort the volume index. Then we used the “Scissors” function in 3D Slicer to remove those areas from the 3D models of crania and DCs. After that, the volumes of the remaining segments of DCs and bone tissues were measured through the “Segment Statistics” function in 3D Slicer.

Because the DC network in humans was mainly found in the frontal, parietal, and occipital bones (García-González et al., 2009; Hershkovitz et al., 1999; Lachkar et al., 2019), we only used the DC volume indices of these bones in the analysis. Although DCs could be found in other

bones (e.g., the zygomatic bone and temporal bone), these cases were rather rare, and thus a quantitative comparison was not feasible. In addition, considering that the DC index of a remaining part of a largely damaged bone may not sufficiently represent that of the original bone, we excluded any bone from the volume analysis if the visual inspection found around one-third of it had been damaged. The better-preserved side of the parietal bones was selected as the representative of the parietal part, given that the distribution of the parietal DCs was generally symmetric (Rangel de Lázaro et al., 2016, 2020).

Concerning the complexity of the DCs, as noted above, it was quantified by measuring the fractal dimensions. The fractal dimension is an index widely applied in biology and medicine, quantifying the complexity of a pattern (Alberich-Bayarri et al., 2010; Bruner et al., 2006; Di leva, 2016; Gutierrez Aceves et al., 2018; Mandelbrot, 1982). In fractal geometry, the fractal dimension of a linear 2D pattern can vary between 1.0 and 2.0. The more complex the vascular network, the higher its fractal dimension. Before performing the fractal analysis, we converted the 3D segments into 2D patterns (Figure 2). This was because all major DC branches, constrained by bone thickness, only extended along the thin diploë that could be seen as a 2D curved surface. With the “Screenshot” function in 3D Slicer, we captured the close-up and orthographic views of every part of a DC model, and each time we only photographed an area smaller than 2 cm². The screenshot pictures must have overlapping fields of view. AutoStitch (Brown & Lowe, 2007) and Adobe Photoshop v2017 (Adobe Inc., San Jose, CA) automatically identified the corresponding features in the overlapping areas to align and match these pictures, which were finally stitched together to form a 2D pattern of an entire DC network. In ImageJ v1.53t (Schneider et al., 2012), the pattern was then converted into a binary image. In some sphere-like areas, such as the parietal eminence, the conversion enlarged the distance between branches, but the branches were not deformed and the degree of complexity was not affected. The fractal dimensions of a binary 2D pattern were finally calculated through the box-counting method with the plugin BoneJ v2 (Domander et al., 2021) in ImageJ.
<figure><img src="image_6.png" /><figcaption>**FIGURE 3** The distribution of the DCs (colored in blue) in the sample of *H. neanderthalensis*, including La Chapelle-aux-Saints 1 (a), La Ferrassie 1 (b), La Quina H5 (c), Spy 1 (d), and Spy 10 (e).</figcaption></figure>

The incomplete DC branches damaged by the taphonomic
processes were excluded and we only conducted fractal analyses on
complete branches. In fractal geometry, the fractal dimension of a ran-
dom and complete branch of a self-similar shape is the same as that of

the entire shape (Di leva, 2016; Mandelbrot, 1982). The vascular
network in humans is considered self-similar (Bruner et al., 2006;
Masters, 2004), and thus, a seriously damaged bone could be included
in the fractal analysis as long as at least one complete DC branch
remains. However, as biological structures, DC networks did not possess perfect self-similarity. Therefore, the fractal dimension of the selected DC branches should be close to but not the same as the general level of entire networks. The fractal analyses in our study were a valuable reference, but for incomplete fossils, their results should be interpreted together with visual inspections.

3 | RESULTS

**3.1 | Distribution and connection patterns**

**3.1.1 | *Homo neanderthalensis***

In the frontal bone, the DC main branches of the selected *H. neanderthalensis* specimens appear in pairs, coursing in the anteroposterior direction (Figure 3). They are distributed in the supraorbital ridge and frontal squama, mainly between the temporal lines. Without exception, the frontal DCs connect to the frontal sinuses and supraorbital foramina in the supraorbital ridge (Figure 4). In the frontal squama, to the exception of La Chapelle-aux-Saints 1, all *H. neanderthalensis* specimens possess DC branches extending into the superior sagittal sinus (SSS) and the small branches of the anterior or middle meningeal vessels (AMV/MMV). In the pterional region, the stems of the MMV anastomose with the frontal DCs in La Chapelle-aux-Saints 1 and with the parietal DCs in Spy 10. In addition, the stems of MMV are linked with the sphenoparietal sinus (SPHS) in La Chapelle-aux-Saints 1 and with the petrosquamous sinus (PSQS) in all *H. neanderthalensis* specimens.

For the parietal DCs, with the exception of Spy 1, all *H. neanderthalensis* specimens manifest a distribution pattern belonging to or similar to the spider type, with most branches radiating from the center of the parietal bone. All *H. neanderthalensis* specimens have dense and microscopic foramina (with diameters smaller than 1 mm)

linking the parietal DCs with the MMV. These foramina are scattered in the whole parietal bone. The superior branches of the parietal DCs in all specimens course parallel to the coronal plane, anastomosing with the SSS at the sagittal suture. The inferior arms of the parietal DCs approach the asterion, connecting to the PSQS in La Chapelle-aux-Saints 1 and La Quina H5 and connecting to the superior petrosal sinus (SPS) in Spy 1 (Figure 5). The connection pattern in the asterio nal region in SPY 10 is ambiguous, as its parietal DCs connect to a narrow and indeterminate branch seeming to lead to the PSQS or the transverse and sigmoid sinus (TSS). But in any case, there is no direct connection between the trunk of the TSS and parietal DCs in the *H. neanderthalensis* sample. In addition, there is no parietal foramen found. The fluid exchange between the parietal DCs and the extra cranial veins in the superior part of the parietal bones happens through many microscopic channels (Figure 6).

The occipital DCs of *H. neanderthalensis* are mainly distributed above the superior nuchal line. They extend into the extra-cranial veins, SSS, TSS, MMV, and PMV (posterior meningeal vessels). Still, Spy 10 is an exception, as its temporal DCs, instead of the occipital DCs, are linked with the TSS at the asterial region.

**3.1.2 | *Homo sapiens***

In the frontal bones of our sample of fossil *H. sapiens*, the DC main branches are distributed symmetrically, draining in the anteroposterior or mediolateral direction (Figure 7). The frontal DC branches extend into the zygomatic bone in Cro-Magnon 1 and into the lesser wing of the sphenoid bone in Abri Pataud. When coursing into the supraorbital foramina and SSS, the frontal DCs of all *H. sapiens* specimens (except Cro-Magnon 1) do not connect with the frontal sinus. Inside the pterional region, the frontal DCs in Abri Pataud, Cro-Magnon 1, and Cro-Magnon 3 connect to the SPHS and/or the stems of the

<figure><img src="image_7.png" /><figcaption>**FIGURE 4** The connection between the DCs and frontal sinus. As an example, in the supraorbital ridge of La Quina H5, the DCs in the frontal bone course anteroposteriorly and connect with the posterior aspect of the frontal sinus. The red arrow marks the connecting point.</figcaption></figure>
<figure><img src="image_8.png" /><figcaption>**FIGURE 5** Different types of connections between the dural sinuses (green) and DCs (blue) surrounding the asterion in the *H. neanderthalensis* and *H. sapiens* samples. In La Quina H5 (a), the parietal DC connects the petrosquamous sinus (PSQS), while the occipital DC connects the transverse and sigmoid sinus (TSS). In Spy 1 (b), the parietal DC anastomoses with the superior petrosal sinus (SPS), and the TSS connects with the occipital DC. In Abri Pataud (c), whose connection pattern at the asterion is shared with other *H. sapiens* specimens, the parietal DC courses directly into the TSS, which has no connection with the occipital DC.</figcaption></figure>

MMV. Outside the pterional region, the frontal DCs of all specimens anastomose with the small branches of the AMV/MMV. In Abri Pataud and Cro-Magnon 1, the stems of the MMV are also linked with the PSQS.

The parietal DCs in *H. sapiens* fossils display various distribution patterns, including the spider type (Abri Pataud), hybrid type (Cro-Magnon 1), coronal type (Cro-Magnon 2), and bonsai type (Cro-Magnon 3). The connection between the parietal DCs and stem of

MMV in the pterional region appears in Cro-Magnon 1, but the link is unobservable in other *H. sapiens* fossils because of the preservation. Outside the pterional region, the parietal DCs in all specimens have a large number of microscopic connecting channels (with diameters smaller than 1 mm) linked with the MMV and extra-cranial veins. The morphology and distribution of these microscopic channels show no difference from those found in *H. neanderthalensis* specimens. The superior part of the parietal DC network extends into the SSS in all
<figure><img src="image_9.png" /><figcaption>FIGURE 6 A microscopic foramen (red circle) links the parietal DC with the extra-cranial veins in La Chapelle-aux-Saints 1.</figcaption></figure>

specimens, while the links between the DCs and parietal foramen appear in Cro-Magnon 1 and 2 (Figure 8). The inferior part of the network in all specimens runs directly into the trunk of TSS in the asterioidal region (Figure 5), where the parietal DCs in Cro-Magnon 1 also anastomose with the mastoid EVs and occipital DCs. The occipital DCs have no connection with the TSS in the asterioidal region, and they extend into the SSS, MMV/ PMV, and extra-cranial veins.

## 3.2 | Size and complexity

Through the visual inspection, we found that the frontal and parietal bones, in all specimens, are more vascularized than the occipital part (Figures 3 and 7). The qualitative inspection also shows that there is no obvious difference between our samples of *H. neanderthalensis* and *H. sapiens*, while considerable variation is found within each taxon.

The volume analysis similarly indicates that the DC volume index is highly variable (Table 2). The DC volume indices of the frontal bones range from 0.8 to 2.2 in our sample of *H. neanderthalensis*, and 0.7 to 1.6 in the sample of fossil *H. sapiens*. The indices of the parietal bones range from 0.8 to 2.8 in the *H. neanderthalensis* sample, and 0.8 to 1.9 in the *H. sapiens* sample. The occipital bones range from 0.3 to 0.8 in the *H. neanderthalensis* sample, and 0.2 to 0.3 in the *H. sapiens* sample. The variation ranges of the fossils belonging to the two taxa largely overlap, and the highest values are systematically found in La Chapelle-aux-Saints 1. Overall, despite the widespread presence of many large DC branches in the neurocranium, the DC networks occupy only a small proportion of the cranial bones.

The fractal analysis also shows that the samples of *H. neanderthalensis* and *H. sapiens* have a similar degree of complexity (Table 3). The fractal dimensions of the frontal DCs vary from 1.47 to 1.55 in our sample of *H. neanderthalensis*, while the dimensions of fossil *H. sapiens* are lower, varying from 1.37 to 1.46. Similarly, *H. sapiens* fossils display a lower level

in the occipital DCs (1.33–1.36) than *H. neanderthalensis* fossils (1.37–1.48). Regarding the parietal region, the ranges of variation of the two samples largely overlap. The dimensions of the parietal DCs range from 1.39 to 1.56 in *H. neanderthalensis* specimens, and from 1.40 to 1.53 in *H. sapiens* specimens.

# 4 | DISCUSSION

## 4.1 | The differences between *H. neanderthalensis* and *H. sapiens*

In our study, the comparison of distribution and connection patterns stresses some differences between our samples of *H. neanderthalensis* and *H. sapiens*. The analysis of distribution patterns finds the pattern of Spy 1 not recorded in any categorization. However, this does not mean that the pattern is species-specific, as there are many indeterminate patterns in *H. sapiens* that have not been documented (Hershkovitz et al., 1999). Among them, we may find an approximation to that of Spy 1. To the exception of Spy 1, all *H. neanderthalensis* specimens possess a spider or spider-like pattern. The spider pattern is a relatively rare pattern found in less than 10% of two extant populations (N = 80, Eisová et al., 2022; N = 108, Hershkovitz et al., 1999). The prevalence of the spider pattern in our sample of *H. neanderthalensis* indicates that its frequency is a possible difference between the two taxa, and we need to expand the sample size in further studies for verification.

For the connection pattern, the DC systems in the *H. neanderthalensis* and *H. sapiens* samples both link the extra-cranial veins, meningeal vessels, and dural sinuses (Figures S2 and S9). When the DC system connects to the extra-cranial network, the frontal DCs in *H. neanderthalensis* fossils travel through the supraorbital ridge, where the DCs always receive tributaries from the frontal sinuses (Figures 4 and 9). By contrast, the links with the frontal sinuses are absent in Abri Pataud, Cro-Magnon 2 and 3. In Cro-Magnon 3, a pair of frontal DC branches course adjacent to the surface of the frontal sinuses without giving off any arms entering the sinuses. As for living *H. sapiens* populations, the incidence of such links is unclear. Only one study on cadaver heads found small DC branches along the superolateral aspect of the frontal sinuses (García-González et al., 2009), but it did not record whether the branches enter the frontal sinuses like those in *H. neanderthalensis*. The size of the frontal sinus is a possible factor influencing the variation of the link. All *H. neanderthalensis* specimens have relatively large frontal sinuses (Balzeau et al., 2022), which means relatively large surface areas of the mucous membranes that may need assistance from the DCs when draining venous blood intra-/ extra-cranially. In addition, we see that Cro-Magnon 1, the individual with frontal sinuses in size comparable to those of *H. neanderthalensis*, has DCs linked with the frontal sinuses, while other *H. sapiens* fossils without such features all have relatively smaller sizes (Balzeau et al., 2022). Future work will have to explore variations for this feature in different hominin species and the potential relationship with the frontal sinus size and shape. Apart from that, the connection of extra-cranial veins with these DCs in the supraorbital ridge does not differ between the samples of *H. neanderthalensis* and *H. sapiens*.
<figure><img src="image_10.png" /><figcaption>**FIGURE 7** The distribution of the DCs (colored in blue) in the sample of *H. sapiens*, including Cro-Magnon 1 (a), Cro-Magnon 2 (b), Cro-Magnon 3 (c), and Abri Pataud (d).</figcaption></figure>

The parietal foramina in *H. sapiens* fossils also link the extra-cranial network with the intra-cranial space, especially with the SSS (Figures 8 and 9). The parietal DCs in modern populations occasionally connect to the parietal foramina (Hershkovitz et al., 1999), and we identify this feature in two fossil *H. sapiens* specimens. By contrast, the parietal foramina are absent in the *H. neanderthalensis* sample. Nevertheless, it does not contradict the fact that there are direct links in *H. neanderthalensis* between the parietal DCs and the extra-cranial network. Without parietal foramina, the links rely on the microscopic foramina scattered in the parietal bones (Figure 6), which are also found in the *H. sapiens* specimens. These microscopic foramina do not differ in morphology and distribution between the two samples.

With respect to the connections between the DC system and the dural sinuses, we see that there is no detectable difference between *H. neanderthalensis* and *H. sapiens* fossils when DCs anastomose with the SSS—the two groups both have dense connecting points along the SSS in the frontal, parietal, and occipital bones. La Chapelle-aux-Saints 1 is an exception for its lack of connecting points in the frontal bone.

The most prominent difference manifests in the connection pattern surrounding the asterion (Figures 5 and 9). Previous studies on extant populations have revealed that the parietal DC branches distributed in the asterional region are always connected to the trunk of the TSS (García-González et al., 2009; Tsutsumi et al., 2013; Yamashiro et al., 2021), and our study confirms this trait in fossil
<figure><img src="image_11.png" /><figcaption>**FIGURE 8** The connection between the parietal foramen and DC. In the parietal bone of Cro-Magnon 1, the parietal foramen leads to the emissary channel coursing intra-cranially, which anastomoses with the parietal DC. The red arrow marks the connecting point.</figcaption></figure>

<table><caption>**TABLE 2** The diploic channel volume indices.</caption><thead><tr><th></th><th>Taxon</th><th>Frontal</th><th>Parietal (the better-preserved side)</th><th>Occipital</th></tr></thead><tbody><tr><td>La Chapelle-aux-Saints 1</td><td><i>H. neanderthalensis</i></td><td>2.2</td><td>2.8</td><td>0.8</td></tr><tr><td>La Ferrassie 1</td><td><i>H. neanderthalensis</i></td><td>-</td><td>0.8</td><td>0.3</td></tr><tr><td>La Quina H5</td><td><i>H. neanderthalensis</i></td><td>0.8</td><td>1.4</td><td>0.5</td></tr><tr><td>Spy 1</td><td><i>H. neanderthalensis</i></td><td>-</td><td>1.3</td><td>0.3</td></tr><tr><td>Spy 10</td><td><i>H. neanderthalensis</i></td><td>1.6</td><td>1.1</td><td>0.7</td></tr><tr><td>Abri Pataud</td><td><i>H. sapiens</i></td><td>1.0</td><td>1.9</td><td>0.2</td></tr><tr><td>Cro-Magnon 1</td><td><i>H. sapiens</i></td><td>1.3</td><td>1.4</td><td>0.3</td></tr><tr><td>Cro-Magnon 2</td><td><i>H. sapiens</i></td><td>0.7</td><td>0.8</td><td>-</td></tr><tr><td>Cro-Magnon 3</td><td><i>H. sapiens</i></td><td>1.6</td><td>1.0</td><td>-</td></tr></tbody></table>

*Note*: Bones damaged severely were excluded in the DC index comparison, as the remaining fragments might not be sufficient to represent the value of the whole bone. For the parietal bones, the better-preserved side was selected for comparison.

<table><caption>**TABLE 3** The fractal dimensions of diploic channels.</caption><thead><tr><th></th><th>Taxon</th><th>Frontal</th><th>Parietal (the better-preserved side)</th><th>Occipital</th></tr></thead><tbody><tr><td>La Chapelle-aux-Saints 1</td><td><i>H. neanderthalensis</i></td><td>1.48</td><td>1.52</td><td>1.48</td></tr><tr><td>La Ferrassie 1</td><td><i>H. neanderthalensis</i></td><td>-</td><td>1.39</td><td>1.43</td></tr><tr><td>La Quina H5</td><td><i>H. neanderthalensis</i></td><td>1.55</td><td>1.44</td><td>1.43</td></tr><tr><td>Spy 1</td><td><i>H. neanderthalensis</i></td><td>-</td><td>1.56</td><td>1.38</td></tr><tr><td>Spy 2</td><td><i>H. neanderthalensis</i></td><td>1.47</td><td>1.51</td><td>1.37</td></tr><tr><td>Abri Pataud</td><td><i>H. sapiens</i></td><td>1.42</td><td>1.40</td><td>1.36</td></tr><tr><td>Cro-Magnon 1</td><td><i>H. sapiens</i></td><td>1.46</td><td>1.53</td><td>1.36</td></tr><tr><td>Cro-Magnon 2</td><td><i>H. sapiens</i></td><td>1.37</td><td>1.41</td><td>1.33</td></tr><tr><td>Cro-Magnon 3</td><td><i>H. sapiens</i></td><td>1.41</td><td>1.40</td><td>1.35</td></tr></tbody></table>

*Note*: Bones without any complete DC branches were excluded from the comparison. For the parietal bones, the better-preserved side was selected for comparison.

*H. sapiens*. The parietal DCs in extant humans may also give off branches into the PSQS or SPS (García-González et al., 2009), but the incidence in extant humans is unknown, and these links never appear

in our *H. sapiens* fossils. In comparison, the parietal DCs of our *H. neanderthalensis* sample never drain directly into the trunk of TSS. Instead, their parietal DCs at the asterion only anastomose with some
<figure><img src="image_12.png" /><figcaption>**FIGURE 9** The connections between the extra-cranial veins (purple), DCs (blue), and dural sinuses (green) in our samples of *H. neanderthalensis* (a) and *H. sapiens* (b), as well as the pattern of the MMV (c, brown) shared between the two taxa. The arrows in (a) and (b) represent the links between the vessels, among which the links only found in one taxon are colored in red. The arrows in (c) indicate the directions of the blood drainage in the vessels.</figcaption></figure>

minor sinuses—the PSQS or SPS. Furthermore, the trunk of the TSS in *H. neanderthalensis* specimens connects to the occipital or temporal DCs in the asterional area, while our sample of *H. sapiens* shows no connection between the TSS and occipital DCs in such area (Figures 5 and 9).

Unlike the extra-cranial network and dural sinuses, when connected with the DCs, the MMV does not differ between our samples of *H. neanderthalensis* and *H. sapiens* (Figure 9). The DCs have consistent connections with the MMV in the pterional region in both samples. This is congruent with previous descriptions of extant populations (García-González et al., 2009; Tsutsumi et al., 2013). Still, our study highlights that there are dense connecting foramina between the DCs and MMV outside the pterional region. These links have not been documented in previous studies on extant populations (García-González et al., 2009; Hershkovitz et al., 1999; Tsutsumi et al., 2013). The small diameters of the foramina (most are smaller than 1 mm) render them unobservable in visual inspections relying on medical CT and MR, but the sizes do not mean that they are rarely of functional significance.

As for the quantitative analyses, our samples of *H. neanderthalensis* and *H. sapiens* share similar DC volume indices and their parietal DCs have similar degrees of complexity (Tables 2 and 3). Moreover, the ranges of fractal dimensions of the frontal and occipital DCs in the *H. neanderthalensis* sample are higher than those in the *H. sapiens* sample (Table 3).

Given the sample size, the difference in fractal dimension is insufficient to justify that *H. neanderthalensis* have more complex frontal and occipital DCs than *H. sapiens*. Still, the evidence from DC indices and fractal dimensions leads to the conclusion that a less developed DC system is not a feature of *H. neanderthalensis*.

Overall, the DCs of the *H. sapiens* and *H. neanderthalensis* specimens have substantial similarities in volume and complexity. The differences between the two samples manifest in the distribution patterns of the parietal DCs and the connection patterns at the frontal sinuses, parietal foramina, and asterional regions. Considering only two species are included in this study, it is unknown whether other hominin species are characterized by unique DC distribution and drainage patterns. Thus, we at this stage cannot highlight the potential utility of the DC in phylogenetic and taxonomic discussions on the hominin lineage. Future studies should investigate the morphology of the DCs in more fossil hominin species and large living populations. However, as the characteristics we found in the *H. neanderthalensis* sample are consistent, the DC shows its potential in distinguishing between *H. neanderthalensis* and *H. sapiens* specimens. This is of interest because many Neandertal-like fossils emerged in the last few decades, while the available evidence from external cranial morphology is not enough to confirm their taxonomic statuses (Li et al., 2017; Martinón-Torres et al., 2017; Wu & Bruner, 2016). In addition, as the DCs are protected by the enclosed space, they sometimes can be
better preserved than the external surface of the cranium. This enhances the application value of the DCs in paleoanthropology.

## 4.2 | The diploic veins and brain evolution

The vascular networks are involved in managing the brain metabolic process, thermoregulation, and intracranial pressure (Bertolizio et al., 2011; Pardridge, 1983; Partington & Farmery, 2014). When the brain morphology and organization change during evolution, the vascular networks, as a supporting system, may adapt as well. However, the possible correlation between brain morphological variation and vessels characteristic during human evolution has not been explored through adequate anatomical evidence.

A major issue of concern is whether and why the encephalization process can influence cranial vascularization. It has been hypothesized that a larger brain tends to have more developed EVs (represented by the emissary foramina), MMVs, and DVs (Falk, 1990; Saban, 1995; Kunz & Iliadis, 2007). However, Braga and Boesch (1997) find the incidence of EVs in robust australopithecines is not higher than in extant apes, even though the former taxon has larger brains. Our findings, together with previous studies (De Stefano & Hauser, 1992; Manzi et al., 2000), find a lower incidence of parietal foramen in *H. neanderthalensis* than in *H. sapiens*, though the two taxa have comparable brain sizes. In addition, by comparing *H. neanderthalensis* and *H. sapiens*, Bruner et al. (2006) show that the former has less complex MMVs. From these, we see much evidence challenging the positive correlation between brain size and the incidence and complexity of EVs and MMVs. In contrast, our samples of *H. neanderthalensis* and *H. sapiens* specimens have comparably developed DC networks. This result does not contradict the hypothesized influence from brain size on DC morphology. In addition, it implies the mechanism behind the intra-species variation of the DCs may be different from those of the EVs and MMVs. Future studies should focus on the hominin species with smaller brain sizes (e.g., *Homo erectus* and *Homo naledi*) and test whether their expression of DVs is different from our samples.

Furthermore, it is still unclear which factor can explain the possible association, if there is any, between the DCs and brain morphology. The most frequently discussed factor is thermoregulation (Eisová et al., 2022; Falk, 1990; Hershkovitz et al., 1999; Rangel de Lázaro et al., 2016). As an organ sensitive to heat, the brain may encounter neurological deterioration when seeing a 1°C increase in cerebral temperature and experiences tissue damage at a temperature over 40°C (Bertolizio et al., 2011; Lieberman, 2011). Falk (1990) argues, in the “radiator theory,” that the evolution of the brain is conditioned by its thermoregulatory system, which is hypothesized by many studies to comprise the EVs, DCs and other veins coursing intra-cranially (Cabanac, 1993; Cabanac & Brinnel, 1985; Falk, 1990; Kunz & Iliadis, 2007). In specific, the venous blood from the scalp cools down during skin heat dissipation, and then it is drained by the veins intra-cranially to help maintain cerebral temperature. The DCs are considered as playing a significant role in this process, since they are a large network distributed all over the neurocranium, and the volume of

blood flow in the DCs is considerable (Cabanac & Brinnel, 1985; Falk, 1990).

The hypothesized thermoregulatory role has been a concern of most anthropological studies on the DC system (Hershkovitz et al., 1999; Rangel de Lázaro et al., 2016, 2020), even though it has been regularly challenged. Brengelmann (1990) doubts the meaning of the DCs, given their minor diameters and low surface-volume ratios are not ideal for efficient heat transfer. Kimbel (1990) and Brengelmann (1990) suggest that the cavernous sinus or cerebral arteries are integral to regulating cerebral temperature. Moreover, damages to the DCs are common in craniotomy, but no thermoregulatory problems have been reported from clinical studies (García-González et al., 2009; Rangel de Lázaro et al., 2020; Yamashiro et al., 2021, 2022).

In our study, fossils attributed to *H. neanderthalensis* and *H. sapiens* both possess a large amount of DC branches linking the extra-cranial space with the intra-cranial vessels. These branches could be the basis of the heat-exchanging function. Moreover, we find a large amount of microscopic draining orifices of the DCs, which can facilitate the drainage and deliver blood to most areas of the extra-/intra-cranial surfaces. Still, these findings cannot justify that the DCs make an essential contribution to brain thermoregulation, nor justify their morphology as a thermoregulatory adaptation to brain evolution.

Future works should include more hominin species and extant populations and use CT data at a resolution at least equivalent to that used in this study. It will thus be possible to document the evolution of the DC system and assess its significance from taxonomic and phylogenetic perspectives, as well as its possible function in thermoregulation. Finally, this may allow us to clarify the role of these structures and to understand their relationship with the internal venous system of the skull, in connection with the functioning of the brain.

## AUTHOR CONTRIBUTIONS

**Jiaming Hui:** Conceptualization (equal); data curation (equal); formal analysis (equal); funding acquisition (supporting); investigation (lead); methodology (lead); project administration (equal); resources (equal); software (lead); supervision (equal); validation (lead); visualization (lead); writing – original draft (lead); writing – review and editing (lead).

**Antoine Balzeau:** Conceptualization (equal); data curation (equal); formal analysis (supporting); funding acquisition (lead); methodology (supporting); project administration (lead); resources (equal); supervision (equal); visualization (supporting); writing – original draft (supporting); writing – review and editing (supporting).

## ACKNOWLEDGMENTS

This study was funded by the China Scholarship Council and French National Research Agency (ANR-20-CE27-0009). The fossil specimens were provided by Musée de l'Homme, a branch of French National Museum of Natural History (MNHN), and Royal Belgian Institute of Natural Sciences (RBINS). The Micro-CT scanning was conducted by the UAR 2700 2AD, MNHN, CNRS, and RBINS. We would like to thank Xiujie Wu, Aurélien Mounier, Jean-Jacques Hublin, Amélie Beaudet, Ameline Bardo, and Patrick Semal for their support. We
also want to thank the editors, editorial board members, and
reviewers for their comments.

DATA AVAILABILITY STATEMENT

Hominin skulls are curated by the French National Museum of Natural History (MNHN) and the Royal Belgian Institute of Natural Sciences (RBINS). Requests for access to the imaging dataset of the MNHN have to be made through the dedicated website (http://colhelper.mnhn.fr/). Requests for the RBINS should be sent to patrick.semal@naturalsciences.be. These institutions are dedicated to the availability of imaging data sets of fossils (Balzeau et al., 2010), and the imaging data used in this study are widely shared among the scientific community. The other data (i.e., 3D models of the DCs) generated in this study are available upon formal request through email to the corresponding author.

ORCID

Jiaming Hui ID https://orcid.org/0000-0002-5408-0857

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## SUPPORTING INFORMATION

Additional supporting information can be found online in the Supporting Information section at the end of this article.

**How to cite this article:** Hui, J., & Balzeau, A. (2023). The diploic venous system in *Homo neanderthalensis* and fossil *Homo sapiens*: A study using high-resolution computed tomography. *American Journal of Biological Anthropology*, 182(3), 412-427. https://doi.org/10.1002/ajpa.24843