The Anatomical Record - 2022 - Richards - Endocranial Anatomy of The Guercy 1 Early Neanderthal From Baume Moula Guercy

Received: 1 August 2022 Revised: 29 October 2022 Accepted: 31 October 2022
DOI: 10.1002/ar.25118
RESEARCH ARTICLE
Endocranial anatomy of the Guercy 1 early Neanderthal

from Baume Moula-Guercy (Soyons, Ardèche, France)
Gary D. Richards 1 | Rebecca S. Jabbour 2 | Gaspard Guipert 3 | Alban Defleur 4
1
Department of Biomedical Sciences,
A. A. Dugoni School of Dentistry, Abstract
University of the Pacific, San Francisco, We provide the first comparative description of the endocranium of the
California, USA
Guercy 1 Early Neanderthal and examine its affinities to Preneanderthals,
2
Department of Biology, Saint Mary's
Neanderthals, and Homo sapiens. The Guercy 1 cranium derives from
College of California, Moraga,
California, USA deposits chronostratigraphically and biostratigraphically dated to the Eemian
3
Institut de Paléontologie Humaine, Interglacial (MIS 5e). For comparative purposes, we compiled a sample of
Fondation Albert Ier Prince de Monaco, European and Southwest Asian subadult and adult Middle-to-Late Pleisto-
Paris, France
4
cene hominins (≈MIS 12–MIS 1; N = 65). We sampled both a Prenean-
CEPAM - UMR 7264 CNRS, Université
de Nice, Nice Cedex 4, France derthal–Neanderthal group and a Homo sapiens group. The Preneanderthal–
Neanderthal group was further divided into three time-successive subgroups
Correspondence
defined by associated MIS stages. Metric and morphological observations
Gary D. Richards, Department of
Biomedical Sciences, A.A. Dugoni School were made on original fossils and physical and virtual endocranial recon-
of Dentistry, University of the Pacific, structions. Guercy 1 and other Early Neanderthals, differ from Prenean-
155 Fifth Street, San Francisco,
CA 94103, USA.
derthals by increased development of the prefrontal cortex, precentral and
Email: grichard@berkeley.edu postcentral gyri, inferior parietal lobule, and frontoparietal operculum. Early
Neanderthal differ, in general, from Late Neanderthals by exhibiting less
Funding information
Arthur A. Dugoni School of Dentistry, development in most of the latter brain structures. The late group addition-
University of the Pacific, San Francisco, ally differentiates itself from the early group by a greater development of the
CA, Grant/Award Number: 03-Activity-
rostral superior parietal lobule, angular gyrus, superior and middle temporal
059; Faculty Development Fund of Saint
Mary's College of California gyri, and caudal branches of the superior temporal gyrus. Endocranial mor-
phology assessed along the Preneanderthal–Neanderthal sequence show that
brain structures prominent in Preneanderthals are accentuated in Early-to-
Late Neanderthals. However, both the Early and Late groups differentiate
themselves by also showing regionally specific changes in brain development.
This pattern of morphological change is consistent with a mosaic pattern of
neural evolution in these Middle-to-Late Pleistocene hominins.
KEYWORDS
Eemian interglacial, Europe, late Paleolithic Homo, Mousterian
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RICHARDS ET AL. 565
1 | INTRODUCTION classic descriptions of recent human and Neanderthal

endocranial anatomy and, most recently, by the qualitative
Since the early days of Neanderthal research, studies of and quantitative assessments of brain to endocranial anat-
endocasts, endocranial morphology, and brain anatomy omy in humans by Dumoncel et al. (2021), who employed
have played a role (Anthony, 1913; Boule, 1909; Boule & modern imaging techniques to demonstrate a consistent
Anthony, 1911; Kappers, 1936). However, there is great correlation between gyral and sulcal patterns and endocra-
variation in fossil preservation and in the detail of pre- nial surfaces.
served endocranial impressions, and identifying soft tis- Identifications of gyri and sulci demonstrate that they
sue anatomical structures from the impressions left on are subject to ontogenetic, idiosyncratic, geographic, and
the endocranium can be difficult (Holloway et al., 2004; sexual variation (Duvernoy, 1999; Keller et al., 2009;
Symington, 1915, 1916). In addition, there is a history of Kobayashi et al., 2018; Le Gros Clark, 1964a; Luders
controversy about the extent to which soft tissue struc- et al., 2004; Symington, 1915, 1916), opening further ave-
tures can be identified from endocrania and how infor- nues of investigation. Beyond observations on gyral and
mative this information is for paleoanthropology sulcal patterns, the analysis of endocasts can also provide
(Holloway, 1985; Neubauer, 2014; Symington, 1915, insights into endocranial shape and volume, brain asym-
1916). For these reasons, the level of anatomical data metries, lobe sizes and orientation, and the ontogeny of
contained in the published record for Middle-to-Late brain–bone relationships (Alatorre Warren et al., 2019;
Pleistocene hominins varies substantially. Well-preserved Balzeau et al., 2014; Bastir et al., 2011; Bruner, 2003, 2004,
Neanderthal cranial remains from Moula-Guercy, 2007, 2008, 2010, 2014, 2018; Bruner, Amano, et al., 2018a;
France, from a layer dated to the Eemian Interglacial Bruner, Averini, & Manzi, 2003a; Bruner, Esteve-Altava, &
(MIS 5e), offer an opportunity to contribute to this lim- Rasskin-Gutman, 2018b; Bruner & Holloway, 2010; Bru-
ited but growing knowledge base and construct a founda- ner, Manzi, & Arsuaga, 2003b; Bruner, Ogihara, &
tion for studying Neanderthal brain anatomy during this Tanabe, 2018c; García-Tabernero et al., 2018;
poorly known and transitional time period. Holloway, 1981a, 1981b; Neubauer et al., 2018; Ogawa
Despite the challenges, the morphology of the endocra- et al., 1970; Pearce et al., 2013; Piveteau, 1970; Poza-Rey
nial cavity forms the basis from which to make inferences et al., 2017; Poza-Rey et al., 2019; Recheis et al., 1999;
about Middle-to-Late Pleistocene Preneanderthal - Nean- Rosas & Bastir, 2020; Wagner, 1935; Weidenreich, 1928).
derthal brain evolution (Alatorre Warren et al., 2019; Further, analysis of the endocranial anatomy provides data
Bakken et al., 2011; Amano et al., 2015; Bruner, 2017; Bru- on the configuration of the dural venous sinuses (Browder
ner, Athreya, et al., 2013; Bruner, Amano, et al., 2018a; et al., 1973; Grimaud-Hervé, 1997, 2004; Grimaud-Hervé &
Bruner, Esteve-Altava, & Rasskin-Gutman, 2018b; Bruner, Saban, 1996; Kopuz et al., 2010; Okudera et al., 1994;
Ogihara, & Tanabe, 2018c; Coqueugniot & Hublin, 2007; Píšova et al., 2017) and middle meningeal neurovascular
de Lumley & Giacobini, 2013; Falk, 2007; Gregory system (Bruner et al., 2009, 2011; Bruner & Sherkat, 2008;
et al., 2017; Grimaud-Hervé, 1997; Gunz et al., 2010; Chandler & Derezinski, 1935; de Lazaro et al., 2018;
Holloway et al., 2004; Hopkins et al., 2015; Kochetkova, Giuffrida-Ruggeri, 1912; Grimaud-Hervé, 1997, 2004;
1978; Morita et al., 2015; Neubauer & Gunz, 2018; Ogihara Grimaud-Hervé & Saban, 1996; Peña-Melian et al., 2011;
et al., 2018; Ponce de Leo n et al., 2021; Rosas et al., 2008; Píšova et al., 2017; Rothman, 1937; Ruíz et al., 2004;
Schoenemann et al., 2007; Sherwood & Bradley, 2019; von Saban, 1979, 1980, 1982, 1984, 1986; Tubbs et al., 2007).
Bonin, 1963; Xiujie et al., 2007; Zollikofer et al., 1995; Zolli- Superficial gyral configurations are minimally corre-
kofer & Ponce de Leo n, 2013). This is due, in part, to a lated with the extent of functional regions, which run
direct relationship between brain and neurocranial size deep to the surface and potentially involve multiple gyri
and shape and the topography of the internal neurocra- (Duvernoy, 1999; Keller et al., 2009; Koutsarnakis
nium, wherein pressure from the developing endocranial et al., 2021; Malikovic et al., 2012; Petrides, 2013;
contents drives neurocranial expansion and osseous Petrides & Pandya, 2012; Sherwood et al., 2003;
imprinting (Bruner, 2007, 2010; Bruner, Averini, & Swenson & Gulledge, 2016; Zelikowsky et al., 2013).
Manzi, 2003a; Bruner, Manzi, & Arsuaga, 2003b; de For these reasons, researchers have largely abandoned
Schotten et al., 2014a, 2014b; Dumoncel et al., 2021; Gunz the practice of correlating specific changes in brain
et al., 2012; Moss, 1997a, 1997b, 1997c, 1997d; function with differences in superficial gyral and sulcal
Neubauer, 2014; Neubauer et al., 2018; Zlatkina & impressions preserved on endocasts (Alatorre Warren
Petrides, 2014). Neural expansion is, however, unevenly et al., 2019; Neubauer, 2014; Schoenemann, 2006).
distributed, and this, in combination with other factors However, while superficial brain anatomy does not cor-
(e.g., meninges, CSF, late growth spurts, etc.), results in relate well with specific brain functions, the description
only some gyri and sulci marking the endocranial surface. and comparison of gyral and sulcal patterns does pro-
This fact was illuminated in Symington's (1915, 1916) vide significant insights regarding the evolution of
566 RICHARDS ET AL.
regional brain structure, which has broad implications cranial remains from Moula-Guercy (Richards
for understanding the evolution of brain function. et al., 2021, 2022) is best accommodated within the
morphological pattern defined for the MIS 7–MIS 5e
Early Neanderthals (Couture & Hublin, 2005; Dean
1.1 | Archeological, stratigraphic, et al., 1998; Guipert et al., 2011; Martínez &
chronological, and paleoenvironmental Arsuaga, 1997; Vandermeersch, 1978). Hominins from
contexts MIS 8 are likely to belong to the Early Neanderthal sub-
group, as well. However, excepting some isolated teeth and
Neanderthal remains from Baume Moula-Guercy a parietal fragment from Payre (Southeastern France:
(Soyons, Ardèche, France) have contributed substantially Moncel & Condemi, 2007; Moncel et al., 2008, 2012;
to the meager European fossil record from MIS 5e Valladas et al., 2008, Condemi et al., 2010), none are
(Eemian/Last Interglacial). Excavations in 1993–1999 by known from MIS 8 (Dean et al., 1998; Hublin, 2002).
A. R. Defleur produced a diverse fauna and flora in direct
association with a Ferrassie Mousterian (Middle Paleo-
lithic) lithic assemblage (Defleur, 1995; Defleur, 2015; 1.3 | Endocranial evidence from
Valensi et al., 2012). Hominin skeletodental remains Preneanderthals and Neanderthals
attributed to a minimum of six individuals (Guercy 1–6:
Richards et al., 2021) were found mixed with the fauna in Early Neanderthals were widely distributed, likely compris-
Layer XV, and many exhibited the impacts of perimortem ing multiple paleodemes (sensu Howell, 1957, 1999). How-
processing consistent with nutritional exploitation ever, cranial remains for this group are rare and
(Defleur, 1995; Defleur et al., 1993; Defleur et al., 1999; fragmentary, and endocranial descriptions are only available
Defleur et al., 2020; Defleur & Desclaux, 2019). Based on for a portion of this sample. Considered by stage, endocast
analysis of the stratigraphy, fauna, and flora, the descriptions for MIS 7 individuals are available for Biache-
hominin-bearing Layer XV is best interpreted as being of Saint-Vaast 1 (Grimaud-Hervé, 1997), Ehringsdorf H
Eemian age (Crégut-Bonnoure et al., 2010; Defleur (Kappers, 1936), and Saccopastore 1 (Bruner & Manzi, 2008;
et al., 2001; Defleur et al., 2020; Manzano, 2015; Payen Sergi, 1913, 1974). For MIS 6, an endocast from the Apidima
et al., 1990; Saos et al., 2014). Assignment of Layer XV to 2 partial cranium has recently been described (de Lumley
MIS 5e is strengthened by absolute dates derived from et al., 2020; Guipert et al., 2019), and detailed comparative
faunal (CSUS/ESR dating) and hominin teeth (laser abla- descriptions are available for the endocrania of the Lazaret
tion U-series dating: Willmes et al., 2016). In further sup- 1 parietal, which is immature and pathologic, and the Laza-
port, the stratigraphically higher Layer VI is associated ret 24 frontal (de Lumley, 1973, 2018; de Lumley et al., 2020;
with the top of MIS 4–base of MIS 3 based on CSUS/ESR de Lumley & Piveteau, 1969; Guipert et al., 2019). Regarding
and thermoluminescence dating (Sanzelle et al., 2000; MIS 5e, material from Bolomor Cave (parietal fragment:
Willmes et al., 2016). Details of the site's stratigraphy, Sarrion, 2006; Arsuaga et al., 2012) and Krapina has been
fauna, flora, dating, and cultural component are provided described. The Croatian MIS 5e material includes the par-
in Defleur et al. (2020) and Richards et al. (2021). tially preserved Krapina 1 subadult (Cofran et al., 2020;
Minugh-Purvis et al., 2000) and the Krapina 3 and 6 adults
(Cofran et al., 2020; Holloway, 1985; Holloway et al., 2004;
1.2 | Subgroups within the Sherwood et al., 2004). The Gibraltar 1 endocast (Grimaud-
Preneanderthal–Neanderthal and Homo Hervé, 1997; Holloway et al., 2004) might also be appropri-
sapiens groups ately included in the Early Neanderthal subgroup, especially
given its morphological similarity to Saccopastore 1 (Bruner,
A morphologically coherent group of European hominins Amano, et al., 2018a; Bruner, Esteve-Altava, & Rasskin-
chronostratigraphically and biostratigraphically associated Gutman, 2018b; Bruner, Ogihara, & Tanabe, 2018c).
with MIS 7–MIS 5e exists within the Neanderthal lineage. Whereas assessments of the endocranial anatomy of
Individuals associated with these MIS stages have been cat- Early Neanderthals are limited to three reasonably com-
egorized as “Preneanderthals” (Elyaqtine, 1995, 1996), plete crania and some partial crania and individual bones,
“recent Preneanderthals” (Rougier, 2003), “Stage 3” the available endocranial descriptions for Preneanderthals
European hominins (included specimens vary, Dean (=MIS 14–MIS 9), Late Neanderthals (=MIS 5d–MIS 3),
et al., 1998; Hublin, 1998), or simply “Neanderthal 1” and Upper Paleolithic Homo sapiens (MIS 3–MIS 2) are
(Martínez & Arsuaga, 1997). Other authors refer to these more numerous. In the case of Preneanderthals, the sample
remains as “Early Neanderthals” (Richards et al., 2021; is geographically and temporally dispersed but mainly
Verna et al., 2010), as is done here. The total morphological represented (76%, 16/21) by the Sima de los Huesos
pattern (sensu Le Gros Clark, 1964a) expressed in the (Atapuerca: Poza-Rey, 2015; Poza-Rey et al., 2017; Poza-
RICHARDS ET AL. 567
Rey et al., 2019) paleodeme, with the remainder compris- (Richards et al., 2021) and endocranium were evaluated
ing Arago XXI/XLVII, Petralona, Reilingen 1, Steinheim with reference to the published literature, photographs,
1, and Swanscombe 1 (Brothwell, 1964; Dean et al., 1998; CT scans, and casts of subadult and adult Homo from the
Grimaud-Hervé, 1997, 1998; Holloway et al., 2004; Middle-to-Late Pleistocene (≈MIS 12–MIS 1) of Europe
Keith, 1938; Le Gros Clark, 1964b; Marston, 1936; Poza-Rey and Southwest Asia. Our comparative sample comprises
et al., 2019; Prossinger et al., 2003). For Late Neanderthals, 66 individuals (Supplementary Data, Table S1), 60 of
the sample includes more complete crania, but comparative which were directly employed in the analysis (Table 1).
endocranial work is dominated by the mostly intact adults La Specimens range from individual bones to nearly com-
Chapelle-aux-Saints 1 (Boule, 1909; Boule & Anthony, 1911; plete crania. In all instances, the accuracy of CT scans
Bruner, Amano, et al., 2018a; Bruner, Esteve-Altava, & and casts was confirmed with reference to published
Rasskin-Gutman, 2018b; Bruner, Ogihara, & Tanabe, 2018c; descriptions, measurements, and photographs of the
Grimaud-Hervé, 1997; Kappers, 1929), La Ferrassie 1 (Bruner, original fossils. We also reference two recent human
Amano, et al., 2018a; Bruner, Esteve-Altava, & Rasskin- samples, one an ontogenetic sample of 5.0–8.0-year-old
Gutman, 2018b; Bruner, Ogihara, & Tanabe, 2018c; crania (N = 69) and the other a sample of preserved
Grimaud-Hervé, 1997; Heim, 1970), La Quina H5 adult cadaver crania and associated brains (N = 20).
(Anthony, 1913; Grimaud-Hervé, 1997; Kappers, 1929, 1934), The juvenile sample is housed in the Center for Dental
and, to a lesser extent, Guattari 1 (Ascenzi, 1991; Bondioli History and Craniofacial Study, and the wet specimens
et al., 1999; Recheis et al., 1999; Sergi, 1974) and the Devil's are in the Department of Biomedical Sciences, both at
Tower 1 subadult (Smith, 1928; Zollikofer et al., 1995). The the A.A. Dugoni School of Dentistry, University of the
Upper Paleolithic Homo sapiens endocranial sample, Pacific.
while containing relatively complete crania, comprises Our fossil comparative sample comprises a
only 12 individuals, with the Předmosti paleodeme Preneanderthal–Neanderthal group and a Homo sapiens
representing 33.3% (4/12) of the sample (Balzeau group (Table 1). The Preneanderthal–Neanderthal
et al., 2013; Bruner, Amano, et al., 2018a; Bruner, group is subdivided into three time-successive sub-
Esteve-Altava, & Rasskin-Gutman, 2018b; Bruner, Ogi- groups based on associated MIS stages as follows: Pre-
hara, & Tanabe, 2018c; Grimaud-Hervé, 1997; Holloway neanderthals (MIS 14–9; N = 21), Early Neanderthals
et al., 2004; Kranioti et al., 2011; Poza-Rey, 2015). (MIS 7–5 e; N = 10), and Late Neanderthals (MIS 5d-3;
Due to the small number of endocranial descriptions N = 16). The H. sapiens group contains remains
available for Early Neanderthals, particularly those from assigned to the Upper Paleolithic (MIS 3–2; N = 12). We
MIS 5e, the endocranium of Guercy 1, a late-stage adoles- placed the chronologically ambiguous Gibraltar 1 (For-
cent female (≈15–16.0 years) from Baume Moula-Guercy, bes' Quarry) in a separate Early–Late Neanderthal group
offers the potential to greatly expand our ability to charac- (Bar-Yosef & Callander, 1999; Coppa et al., 2005;
terize temporal and geographic variation in brain mor- Stringer, 2000).
phology among European hominins and to study Determination of the developmental age and sex of
evolutionary changes in European hominins during the Guercy 1 is detailed in Richards et al. (2021). We con-
Last Interglacial (MIS 5e), a time of climate change. We cluded that Guercy 1 represents the remains of a late-
here provide a comparative description of the endocra- stage adolescent female with a developmental age of
nium of Guercy 1, in which comparisons of the original ≈15–16.0 years ±6 months.
fossil and a virtual endocast are made with members of
the Preneanderthal–Neanderthal group and the Upper
Paleolithic Homo sapiens group. Our anatomical compari- 2.2 | Definitions: Endocranial points,
sons include observations on general shape characteristics measures, gyri, sulci, and vascular
of the frontal and parietal lobes and on the configurations impressions
of specific sulci and gyri, middle meningeal neurovascular
impressions, dural sinuses, and lateral lacunae. In the few instances where standard metric dimensions
can be measured, we employ the definitions and point
locations used by Bruner and Manzi (2008) and Poza-Rey
2 | MATERIALS AND METHODS (2015). Identification of gyri and sulci follows the works
of Duvernoy (1999), Badre (2008), Keller et al. (2009),
2.1 | Materials Petrides and Pandya (2012), Petrides (2013), and Zlatkina
and Petrides (2014). Assessment and categorization of
For descriptive and comparative purposes, the Guercy the middle meningeal neurovascular grooves follows
1 fossil and virtual reconstructions of the cranium Adachi (1928).
568 RICHARDS ET AL.
T A B L E 1 Listing of Preneanderthal—Neanderthal and upper Paleolithic Homo sapiens specimens with endocranial descriptions
employed or referenced in this studya
Age
Specimen(s) group MIS Stageb Subgroupc References
d
Arago XXI/XLVII Adult 12 Preneanderthal Grimaud-Hervé (1997, 1998); Holloway et al. (2004)
Petralona 1 e Adult 12/11; 8–6 Preneanderthal Demuro et al., 2019; Grün, 1996; Poza-Rey (2015)
Reilingen 1 Adult 9(?) Preneanderthal Dean et al. (1998)
Sima de los Huesos Adult 12/11 Preneanderthal Poza-Rey (2015); Poza-Rey et al. (2017, 2019)
SH2, SH4-5, SH8-SH17
Sima de los Huesos Subadult 12/11 Preneanderthal Poza-Rey (2015); Poza-Rey et al. (2017, 2019)
SH3, SH6-7
Steinheim 1 Adult 9(?) Preneanderthal Prossinger et al. (2003)
Swanscombe 1 Adult 11 Preneanderthal Keith (1938); Marston (1936); Brothwell (1964); Le
Gros Clark (1964b)
Apidima 2f Adult Base 6 Early Neanderthal Guipert et al. (2019); de Lumley et al. (2020)
Biache-Saint-Vaast 1 Adult 7a Early Neanderthal Grimaud-Hervé (1997)
Bolomor HCB-07g Adult 5e Early Neanderthal Sarri
on (2006); Arsuaga et al. (2012)
Ehringsdorf H(9) Adult 7 Early Neanderthal Kappers (1936); Vlček, 1993; Grimaud-Hervé
(1997); Holloway (1981a)
Krapina 1 Subadult 5e Early Neanderthal Minugh-Purvis et al. (2000); Cofran et al. (2020)
Krapina 3(C) Adult 5e Early Neanderthal Holloway (1985); Holloway et al. (2004); Sherwood
et al. (2004); Cofran et al. (2020)
Krapina 6(E) Adult 5e Early Neanderthal Holloway (1985); Holloway et al. (2004); Sherwood
et al. (2004); Cofran et al. (2020)
Lazaret 1(+2) Subadult 6 Early Neanderthal Piveteau (1967); de Lumley and Piveteau (1969); de
Lumley (2018)
Lazaret 24 Adult 6 Early Neanderthal de Lumley and Piveteau (1969); de Lumley (2018)
Saccopastore 1 Adult 7 Early Neanderthal Sergi (1913, 1974); Bruner and Manzi (2008)
Gibraltar 1 Adult ? Early/Late Neanderthal Grimaud-Hervé (1997); Holloway et al. (2004)
Amud 1 Adult 4–3; Base 2(?) Late Neanderthal Ogawa et al. (1970); Holloway et al. (2004)
Carigüela II Subadult 4–2 Late Neanderthal de Lumley (1973); Jiménez-Arenas et al. (2019)
Cova Negra, Parietal 1 Adult 5b-3 Late Neanderthal de Lumley (1973)
Engis 2 Subadult 3–2 Late Neanderthal Grimaud-Hervé (1997)
Feldhofer 1 Adult 3 Late Neanderthal Boule (1909); Kappers (1936); Holloway et al.
(2004); Grimaud-Hervé (1997)
Ganovceh Adult Top 5e/Base 5d Late Neanderthal (?) Vlček (1955); Eisova et al. (2019)
Devil's Tower 1 Subadult Top 3/Base 2 Late Neanderthal Smith (1928); Zollikofer et al. (1995)
Guattari 1 (Monte Adult 3–2 Late Neanderthal Sergi (1974); Ascenzi (1991); Recheis et al. (1999)
Circeo)
La Chapelle-aux- Adult 5d-3 Late Neanderthal Boule and Anthony (1911); Kappers (1929);
Saints 1 Grimaud-Hervé (1997); Bruner, Amano, et al.
(2018a); Bruner, Esteve-Altava, and Rasskin-
Gutman (2018b); Bruner, Ogihara, and Tanabe
(2018c)
La Ferrassie 1 Adult 3 Late Neanderthal Heim (1970); Grimaud-Hervé (1997); Bruner,
Amano, et al. (2018a); Bruner, Esteve-Altava, and
Rasskin-Gutman (2018b); Bruner, Ogihara, and
Tanabe (2018c)
Le Moustier 1 Adult 3 Late Neanderthal Grimaud-Hervé (1997); Holloway et al. (2004)
RICHARDS ET AL. 569
TABLE 1 (Continued)
Age
Specimen(s) group MIS Stageb Subgroupc References
La Quina H5 Adult 3(?) Late Neanderthal Anthony (1913); Kappers (1929); Grimaud-Hervé
(1997)
Salzgitter-Lebenstedt 1 Adult Base 5–3 Late Neanderthal Hublin (1984)
Spy I Adult 3 Late Neanderthal Holloway (1981a, 1981b)
Spy II Adult 3 Late Neanderthal Holloway (1981a, 1981b)
Teshik Tash 1 Juvenile 3–2(?) Late Neanderthal Grimaud-Hervé (1997); Holloway et al. (2004);
Poza-Rey (2015)
Brno 3 Adult 2 Upper Paleolithic H. s. Grimaud-Hervé (1997)
Cioclovina 1 Adult Top 2 Upper Paleolithic H. s. Kranioti et al. (2011)
Cro-Magnon I Adult 2–1 Upper Paleolithic H. s. Balzeau et al. (2013); Bruner, Amano, et al. (2018a);
Bruner, Esteve-Altava, and Rasskin-Gutman
(2018b); Bruner, Ogihara, and Tanabe (2018c)
Cro-Magnon III Adult 2–1 Upper Paleolithic H. s. Grimaud-Hervé (1997); Holloway et al. (2004)
Dolní Vĕstonice I Adult 3 Upper Paleolithic H. s. Grimaud-Hervé (1997); Poza-Rey (2015)
Dolní Vĕstonice II Adult 3 Upper Paleolithic H. s. Grimaud-Hervé (1997); Poza-Rey (2015)
Dolní Vĕstonice III Adult 3 Upper Paleolithic H. s. Holloway et al. (2004); Poza-Rey (2015)
Mladeč 1 Adult Base 3 Upper Paleolithic H. s. Bruner, Amano, et al. (2018a); Bruner, Esteve-
Altava, and Rasskin-Gutman (2018b); Bruner,
Ogihara, and Tanabe (2018c)
Předmosti 3 Adult Top 2/Base 1 Upper Paleolithic H. s. Grimaud-Hervé (1997); Holloway et al. (2004);
Poza-Rey (2015)
Poza-Rey (2015)
Poza-Rey (2015)
Poza-Rey (2015)
a
This listing includes mostly complete crania, partial crania, and individual bones.
b
References regarding site dating can be found in Supplementary Data, Table S1.
c
Refer to the Materials section for the range of MIS stages associated with each chronostratigraphic subgroup.
d
Description of the endocranial anatomy derives from a composite of two individuals, Arago XXI (frontofacial region) and Arago XLVII (isolated parietal).
e
Metric values for the endocranium derive from Poza-Rey (2015). However, anatomical details of the endocast do not appear to be available.
f
Early Neanderthals are defined as having a biostratigraphic and chronostratigraphic association with MIS 7–MIS 5e. Apidima 1 and 2 have a published
association with the base of MIS 6 that associates them with the Early Neanderthal subgroup. However, Harvati et al. (2019) suggest that Apidima 1 has a
cranial vault morphology that is like early anatomically modern Homo sapiens. Alternatively, Guipert et al. (2019), de Lumley et al. (2020), Rosas and Bastir
(2020), and the current authors consider both Apidima 1 and 2 to possess a derived suite of characters that associates them with the Neanderthal group. The
endocranium of Apidima 1 has not been described.
g
Description limited to the endocranial surface of Bolomor HCB-07. An endocast has not been produced.
h
230Th dating of the Ganovce endocast provided an absolute date of 105 ka (+10.2 ka, 9.4 ka: Jäger, 1989), which is consistent with results of fluorine
absorption dating (≈100 ka; Vlček & Pelikan, 1956). The fauna from Layers D-E (endocast associated with Layer D) contains a combination of forest and steppe
elements. The underlying Layer C contains a warm phase forest fauna with forest elephant and rhinoceros, while the overlying Layer F contains a Weichselian
glacial fauna (Eisova et al., 2019). Taken together, these data have suggested an association of the Ganovce endocast with MIS 5, generally, and the top of MIS
5e–base of MIS 5d, specifically.
2.3 | CT scan parameters and virtual Hôpital Privé Pasteur, Radiology Unit, Guilherand
reconstruction Granges, France. CT-slice and interslice thicknesses
are 0.625 and 0.3 mm, respectively, and the resulting
Computed tomography (CT) scanning was carried out pixel spacing is 0.4883 0.4883 mm2. Refer to
with a General Electric (GE) BrightSpeed scanner at Richards et al. (2021) for further details of the
570 RICHARDS ET AL.
scanning parameters and reconstruction of the Guercy TABLE 2 List of abbreviations of brain structures
1 cranium.
Abbreviation Brain structure
The Guercy 1 endocranium was virtually recon-
acsfs Accessory superior frontal sulcus
structed in Amira (6.5) following techniques discussed in
Zollikofer and Ponce de Le on (2005), Russ (2011), and AnG Angular gyrus
Weber and Bookstein (2011). In brief, semi-automated cs Central sulcus
and manual segmentation of the endocranial surface of IFG Inferior frontal gyrus
the Guercy 1 reconstruction was accomplished in Amira ifs Inferior frontal sulcus
by first extracting a volume from the merged surface
imfs-h Intermediate frontal sulcus—horizontal
model. During the extraction process, the pixel count was
imfs-v Intermediate frontal sulcus—vertical
reduced by 25% to yield isotropic voxels of ≈0.16 mm3.
This voxel size yields a morphologically and dimension- IPL Inferior parietal lobule
ally accurate model. Higher pixel counts were tested, but IPOG Inferior parieto-occipital gyri
these resulted in unacceptably high slice counts (requir- ls Lateral sulcus (Sylvian fissure)
ing excessive computer processor/memory usage) with MFG Middle frontal gyrus
no appreciable increase in detail or dimensional accu- PiPG Posterior inferior parietal gyrus
racy. The endocranial surface model employed in this
PoCG Postcentral gyrus
analysis and figured herein comprises the original seg-
pocs Postcentral sulcus
mented surface; no smoothing routines were applied. All
observations and comparisons were made on isosurface PrCG Precentral gyrus
renderings of the virtual surface model. Such renderings prcs Precentral sulcus
have been shown to provide a highly accurate surface SFG Superior frontal gyrus
model (Balanoff et al., 2016). Middle meningeal neuro- sfpms Superior frontal paramedian (paramidline)
vascular patterns for both Guercy 1 and our recent juve- sulcus
nile sample were reconstructed by plotting 3D landmarks sfs Superior frontal sulcus
of varying point sizes in the endocranial impressions. For
sfs-a Anterior portion of superior frontal sulcus
illustrative purposes, landmark sets were replaced with
sfs-p Posterior portion of superior frontal sulcus
2D tubes in Adobe Illustrator.
SMG Superior marginal gyrus
SPL Superior parietal lobule
3 | R E SUL T S
hemisphere of other fossil specimens, with the under-
3.1 | Endocranial morphology standing that asymmetries in the brain are expected.
Unless otherwise noted, all gyri and sulci described
Endocranial surfaces of Guercy 1, a late-stage adolescent herein are clearly marked on the Guercy 1 endocranial
female, are well preserved, and only a few small regions surface/endocast. Gyri and sulci that were fragmented or
of cortex are missing or damaged (Richards et al., 2021). obscured are not included in the description.
Details of general shape, sulci and gyri, middle menin-
geal neurovascular impressions, and dural sinuses and
lateral lacunae are compared with those from adolescent 3.2 | Frontal lobe morphology
and adult Preneanderthals, Neanderthals, and Upper
Paleolithic and recent H. sapiens. Refer to Table 2 for a In a superior view, the left superior and middle frontal
list of abbreviations for gyri, sulci, and other neural gyri (SFG and MFG, respectively) are missing their
structures. rostral-most extent. The SFG is separated from the MFG
In the following description, we use terms such as by a deep and wide impression that represents the supe-
expanded, inflated, and developed to convey relative rior frontal sulcus (sfs: Figure 1a–c). In Guercy 1, Apidima
sizes, or degrees of projection, of gyri that have left 2 (Guipert et al., 2019), La Quina H5 (Anthony, 1913),
impressions on the endocranial surface. These terms do and recent humans, the sfs runs a relatively horizontal
not imply changes in brain function; they simply describe (parasagittal) course. In recent humans, the sfs is gener-
morphology. Further, given that Guercy 1 preserves ally not a continuous sulcus; it is divided into an anterior
mainly the left side of the neurocranium, our observa- sulcus (sfs-a) and a posterior sulcus (sfs-p: Petrides &
tions relate to this hemisphere of the brain. In some Pandya, 2012). This is also the case in Guercy 1, wherein
cases, we have made comparisons with the right the caudal end of the sfs-p arises from the rostral aspect
RICHARDS ET AL. 571
F I G U R E 1 (a–c) Lateral (a), three-quarters (b), and superior (c) views of the Guercy 1 endocranial reconstruction. Inset figure shows
the Guercy 1 endocast on a reshaped endocast of the late Neanderthal La Ferrassie 1. aarlf, anterior ascending ramus of lateral fissure
(sulcus); acsfs, accessory superior frontal sulcus; AnG, angular gyrus; Br, Broca's area (areas 44–45); cs, central sulcus; f1, superior frontal
lobe; f2, middle frontal lobe; f3, inferior frontal lobe; half, horizontal ascending ramus of lateral fissure (sulcus); ifs, inferior frontal sulcus;
imfs-h, intermediate frontal sulcus-horizontal; imfs-v, intermediate frontal sulcus-vertical; IPL, inferior parietal lobule; ips, intermediate
parietal sulcus; ls, lateral sulcus; LonFis, longitudinal fissure; pimfs-d, paraintermediate frontal sulcus-dorsal; pimfs-v, paraintermediate
frontal sulcus-ventral; PoCG, postcentral gyrus; porb, pars orbitalis (area 47), PrCG, precentral gyrus; prcs, precentral sulcus; prts,
pretriangular sulcus; ptr, pars triangularis (area 45); pop, pars opercularis (area 44); sfpms, superior frontal paramedian sulcus; sfs-a, superior
frontal sulcus-anterior; sfs-p, superior frontal sulcus-posterior; SMG, superior marginal gyrus; STG, superior temporal gyrus; SupSS, superior
sagittal sinus; Ts, triangular sulcus. Terminology and abbreviations follow Petrides (2013)
of the precentral sulcus (prcs) and continues rostrally configuration in recent humans (Petrides & Pandya, 2012).
along the ventral aspect of a V-shaped impression What appears in Guercy 1 and Apidima 2 as a rostral
(Figure 1b, c). This impression denotes the intersection of elongation of the sfs (de Lumley et al., 2020; Guipert
the sfs-p and superior frontal paramedian sulcus (sfpms; et al., 2019) is likely an accessory superior frontal sulcus
Petrides & Pandya, 2012). The sfs-a continues from the (acsfs, sensu Petrides & Pandya, 2012), as the sfs in
rostral extent of the sfs-p, crosses the coronal suture, and recent humans does not generally extend to the rostral
ends as it curves medially around the rostral end of a surface of the frontal lobe (Figure 1b, c: Petrides &
prominent paramedian section of the SFG (Figure 1b, c). A Pandya, 2012). Rostral to the sfs-a in humans lies the
similar medial deviation of the rostral aspect of the sfs-a acsfs medially and the horizontal portion of the inter-
occurs in Apidima 2 (de Lumley et al., 2020; Guipert mediate frontal sulcus (imfs-h) laterally.
et al., 2019), Feldhofer 1 (Anthony, 1913), and Devil's A thickened paramedian section of the left SFG is
Tower 1 (Grimaud-Hervé, 1997) and is a typical apparent alongside the midline. The gyrus is divided
572 RICHARDS ET AL.
centrally by the coronal suture and split dorsoventrally into relative to La Chapelle-aux-Saints 1, as discussed further
two regions by the sfpms (Figure 1b, c). The caudal extent below (Figure 2c).
of the sfpms merges with the caudal aspect of the sfs-p and In lateral view, the inferior frontal sulcus (ifs) of
forms the superior arm of the V-shaped impression Guercy 1 delimits a well-defined IFG (Figure 1a, b). This
described above (Figure 1b, c). Only the Sima de los Hue- gyrus includes those portions defined cytoarchitecturally
sos SH-3 Preneanderthal (Poza-Rey, 2015) and the La by Brodmann (1909) as areas 44 (pars opercularis),
Chapelle-aux-Saints 1 Late Neanderthal (Grimaud- 45 (pars triangularis), and 47 (pars orbitalis). Note that
Hervé, 1997) endocasts suggest a morphology similar to Brodmann's areas 44 and 45 correspond to that region of
this region of the SFG. However, expansion of the frontal the frontal lobe identified generally as Broca's area
venous lacuna obscures gyral impressions in this region, as (Aboitiz & Garcia, 1997; Sherwood et al., 2003), whereas
also observed by Symington (1915). As discussed further the so-called “Broca's cap” approximates areas 44, 45,
below, the frontal lobe of Guercy 1 is rostrocaudally short, and 47 of Brodmann (Bruner & Holloway, 2010; Keller
but the shortness does not appear to have impacted the et al., 2009; Schoenemann, 2006). Differences in these
spatial relationship between the venous lacuna, the coronal terms are important for understanding the morphology
suture, and this region of the SFG. However, there is some
uncovering of the SFG in this region due to a right-side
deviation of the superior sagittal sinus and frontal lateral
lacuna in Guercy 1. This altered course of the sinus is likely
related to a slight right-side deviation of the anterior sagit-
tal suture (Richards et al., 2021), a feature also seen in La
Quina H5. Impressions on the preserved right frontal
squama show that the SFG, sfs, and sfpms were similarly
configured and developed bilaterally (Figure 1c). The SFG,
sfs, and related structures are difficult to discern on the
Late Neanderthals La Chapelle-aux-Saints 1 and La Ferras-
sie 1, although a portion of the sfs-a is visible on both La
Ferrassie 1 (=sillon frontal supérieur, Heim, 1970) and La
Quina H5 (Anthony, 1913).
The left impression for the SFG is paralleled by the
dorsal extent of the MFG (Figure 1a–c). Guercy 1 pre-
serves only a small section of the right MFG, but the pre-
served SFG and MFG are equally developed and
bilaterally similar to those in Saccopastore 1 (Bruner &
Manzi, 2008). In the Late Neanderthals La Chapelle-aux-
Saints 1 and La Ferrassie 1, the MFG and associated sulci
are slightly more apparent on the right than the left side.
In Guercy 1 and Saccopastore 1, the development of these
gyri is localized and does not involve their full extent
(Figure 1a, b). In both La Chapelle-aux-Saints 1 and La
Ferrassie 1, the SFG and MFG tend to be more developed
throughout their length, a feature of these Late Neander-
thals noted by Kappers (1929). The greater expansion of
these frontal gyri in the Late group results in more evenly
impressed gyri and, resultingly, less sulcal detail. Further,
the dorsal aspect of the IFG and ventral aspect of the
MFG, together comprising portions of the lateral fronto-
polar, ventrolateral, and dorsolateral prefrontal cortex
(sensu Badre, 2008), project more laterally in Late Nean-
derthals relative to Guercy 1. This expansion results in a
slight “step” in the coronal cross-section in the region of
the IFG and MFG in many Late Neanderthals, with La
Ferrassie 1 and Amud 1 having a less-developed “step” FIGURE 2 Legend on next page.
RICHARDS ET AL. 573
of Guercy 1, wherein the components of the Broca' cap flat and medially retreating (Figure 1a–c). In La Ferrassie
are differentially developed. Note also that the Broca's 1, the lateral expansion and resulting convexity of the
cap forms a major portion of the ventrolateral prefrontal pars orbitalis–pars opercularis region is less marked than
cortex (Badre, 2008). in La Chapelle-aux-Saints 1, but in both Late Neander-
When Guercy 1 is considered in an anterior view, the thals the region is more convex and laterally projecting
lateral development of the left pars orbitalis is seen to relative to the Early Neanderthals (Figures 2c and 3a–c).
reach its maximum at its ventral-most point (i.e., contact Comparing the maximum breadth between Broca's
surface with the orbital plate), with the IFG retreating caps in Guercy 1 with values for La Chapelle-aux-Saints
dorsomedially as the level of the pars opercularis is 1 and La Ferrassie 1 shows them to be similarly broad
approximated (Figures 1b and 3a). The morphology of (Table S2). However, the measurement for these Late
Apidima 2 and Saccopastore 1 are similar, although in Neanderthal specimens was taken in a more dorsal posi-
both cases there is slightly more lateral development just tion than for Guercy 1, consistent with the most lateral
dorsal to the pars orbitalis relative to that in Guercy points of their Broca's caps. The position of the measure-
1. This morphological difference may be due to the short ment in Early Neanderthals Apidima 2 and Saccopastore
frontal of Guercy 1, implying a packaging issue and not 1 is slightly dorsal to that in Guercy 1, but it is still ven-
differential neural development. The pars orbitalis in La tral to that in the La Chapelle-aux-Saints 1 and La Ferras-
Chapelle-aux-Saints 1 and La Ferrassie 1 forms the sie 1 Late Neanderthals.
ventral-most portion of a broad swelling that includes the In coronal section, the endocranial surface corre-
laterally projecting pars triangularis and pars opercularis sponding to the frontal lobe in Guercy 1 describes a long,
(Figure 3c). In lateral view, these regions, comprising shallow arc from the pars orbitalis to the midline
Broca's cap, form a portion of the IFG that is rostrocaud- (Figure 3). In the Sima de los Huesos Preneanderthal
ally wide, relative to Guercy 1, and dorsoventrally con- endocasts (cf. SH-3, SH-4, SH-5), the endocranial profile
vex. Guercy 1 differs from this morphology, as there is in this view is like that in Guercy 1, as it retreats medially
only minor lateral expansion of the pars orbitalis, and from the ventrolateral prefrontal cortex (Poza-Rey, 2015;
this expansion is limited to its ventral-most region. Fur- Poza-Rey et al., 2019). However, in these endocasts the
ther, Guercy 1 has only minor lateral development of the MFG and ventrolateral aspect of the SFG are less
ventral-most pars triangularis, and the pars opercularis is expanded, while the midline aspect of the SFG and dural
sinuses are more prominent, creating a midsagittal peak.
The level of development of these gyri results in a slight
concavity in the prefrontal (=ventrolateral and dorsolat-
F I G U R E 2 (a–c) Lateral and superior views of (a) Guercy eral cortex) and premotor (=portions of the anterior and
1, (b) La Ferrassie 1, and (c) La Chapelle-aux-saints 1. In (a), the ventral cortex) regions, and it is readily apparent on the
Guercy 1 endocast is positioned on a reshaped endocast of La left side of SH-4, SH-5, SH-10, and SH-14. In the Early
Ferrassie 1 (reduced in height, breadth, and shortened slightly) for
Neanderthals Apidima 2 and Saccopastore 1, as in
illustrative purposes. Note that the Broca's cap in Guercy 1 only
Guercy 1, these regions of the prefrontal and premotor
extends ventrally to (1) and not to that depicted for the reshaped La
cortices are more expanded relative to the Prenean-
Ferrassie 1 endocast. In (a), the Guercy 1 ventral-most pars orbitalis
is marked at (1) and coincides with the lateral-most point of the derthal condition (cf. SH-4, SH-5), and the midsagittal
Broca's cap, as denoted at (2). Note in (b and c) the more peaking is less marked, resulting in a smoother coronal
dorsolateral positioning of the lateral-most Broca's cap in late curvature. Lack of a concavity of the prefrontal and pre-
Neanderthals. At (3) note the slight “step” in the coronal outline of motor cortex was also noted by Smith (1928) in Devil's
the late Neanderthals' frontal lobes. Distortion of the La Ferrassie Tower 1. In the Late Neanderthals La Chapelle-aux-
1 endocast at (3) gives the appearance of a slightly greater offset Saints 1 and La Ferrassie 1, the coronal section differs. In
than exists. Guercy 1 lacks this inflation of the inferior frontal lobe. these individuals, the lateral frontopolar and inferior por-
In (a) and (b) observe the different profiles of the superior and tions of the ventrolateral prefrontal cortex initially extend
lateral endocast. The vertex is noted at (4), while the point at which laterally from the pars orbitalis to reach their lateral-most
the flattened region of the parietal lobe begins to sharply angle
extent on the mid-to-upper portion of the pars triangu-
posteroinferiorly is noted at (5). Guercy 1, and other early
laris—pars opercularis, as also observed in anterior view.
Neanderthals, lack the distinct angulation near the vertex (4), and
they have a shorter distance between the vertex and the point of
Dorsal to this region, expansion of the frontal lobe results
angular change in the parietal lobe (5) when compared with late in a more vertical orientation of the lobe dorsal to the
Neanderthals. The lateral contour of the frontoparietal is depicted IFG, with the surface being flattened or slightly concave
at (6) for Guercy 1 and a late Neanderthal (La Ferrassie 1). Note the compared with the convex and medially retreating sur-
rounded oval shape of the Guercy 1 endocast relative to the more face in Early Neanderthals. This region gives way to a
angular shape of late Neanderthals slight peaking of the SFG and dural sinuses in the
574 RICHARDS ET AL.
F I G U R E 3 (a–c) Coronal sections through the maximum breadth at Broca's caps in (a) Guercy 1, (b) La Ferrassie 1, and (c) La
Chapelle-aux-saints 1. The La Ferrassie 1 section has been flipped horizontally due to damage to the left side. In the figures, (1) denotes the
widest point of the Broca's caps. The red arrows denote the inferolateral-most extent of the pars orbitalis. Note at (2) how Guercy 1 has a
smooth curvature while La Ferrassie 1 and La Chapelle-aux saints 1 have a greater expansion of the inferior frontal lobe that results in a
slight step in the contour. Guercy 1 has a low and continuous curvature through the middle frontal gyrus (3) and into the superior frontal
gyrus and sagittal sinus (4). Alternatively, La Ferrassie 1 and La Chapelle-aux-saints 1 have more vertically oriented profiles that rise steeply
between (1–2) and (3–4), with the latter section being flat to slightly convex, and they have a slight peak at the superior frontal gyri and
superior sagittal sinus (4)
midsagittal region (Figures 2c and 3a–c). In La Ferrassie more projecting and dorsoventrally convex. Saccopastore
1 and Amud 1, the endocasts exhibit a slight convexity in 1 has a slightly more inflated pars opercularis–pars trian-
the dorsolateral prefrontal cortex. The La Chapelle-aux- gularis region relative to Guercy 1, but it is like Guercy
Saints 1 endocast does not share this convexity, as it is 1 in angling caudoventrally. In the Late Neanderthals La
slightly concave to flat in this region (Figure 3c). How- Chappelle-aux-Saints 1 and La Ferrassie 1, the pars oper-
ever, this difference might be explained by advanced indi- cularis–pars triangularis region is more inflated and ros-
vidual age rather than by a lack of neural development. It trally inclined (rotated anticlockwise) relative to Guercy
is well known that this portion of the prefrontal cortex in 1. In recent humans, the pars opercularis is usually verti-
recent humans undergoes the greatest reduction in vol- cally (dorsoventrally) oriented. However, it is also fre-
ume, thickness, and surface area with age (Lemaitre quently divisible into a rostral and a caudal portion, with
et al., 2012). The shift in these Late Neanderthals to pre- the latter variably submerged into the inferior precentral
frontal and premotor cortices that have expanded both sulcus (Petrides & Pandya, 2012). In Guercy 1, the pars
dorsally and laterally, with slightly convex to flat sur- opercularis does not appear to be submerged into the
faces, shows that this region of the frontal lobe was less inferior precentral sulcus, because it extends caudally as
developed in both Preneanderthals and Early Neander- a distinct and undivided swelling. Further, at its caudal-
thals. In these Late Neanderthals, this region of the fron- most extent the pars opercularis appears to continue
tal lobe is less developed relative to that of Upper across the inferior precentral sulcus to merge into the
Paleolithic (cf. Cioclovina 1, Cro Magnon 1, Předmosti PrCG at its inferior aspect. This region is damaged in
3, 4, 9) and recent humans, as also observed by Kranioti Biache Saint Vaast 2, but morphology like that in Guercy
et al. (2011). 1 appears to be present in both Apidima 2 and Saccopas-
In lateral view, the pars opercularis in Guercy 1 com- tore 1, as it is in some Sima de los Huesos Prenean-
prises a roughly ovate region that (1) is mostly rostral to derthals (cf. SH-4, Poza-Rey, 2015). Further comparisons
the coronal suture, (2) parallels the course of the suture, are needed, however, to clarify these gyral and sulcal
such that it inclines caudodorsally, and (3) protrudes only relationships.
slightly (Figure 1a, b). In the Sima de los Huesos Pre-
neanderthals, the morphology of the pars opercularis var-
ies (Poza-Rey, 2015; Poza-Rey et al., 2019), but it appears 3.3 | Parietotemporal lobe morphology
to be similar in its orientation and degree of inflation to
that expressed in Guercy 1. In the Early Neanderthal Api- The anterior ascending and anterior horizontal rami
dima 2, although the pars orbitalis and pars triangularis (=branche présylvienne postérieure et antérieure, respec-
are weakly inflated as in Guercy 1, the pars opercularis is tively, sensu Boule & Anthony, 1911) of the lateral sulcus
RICHARDS ET AL. 575
(ls, =Sylvian or lateral fissure) are missing only their con- the greater expansion of the parietal lobe (=inferior pari-
nection to the ls in Guercy 1 (Figure 1a, b). The ventral etal lobule, IPL) and second and third caudal branches of
border of the ls (=posterior ramus ls) is weakly demar- the STG and the MTG in the late group.
cated by the superior temporal gyrus (STG), but the sul- The precentral sulcus (prcs, =sillon pre-central, pre-
cus can be followed to near its caudal end (Figure 1a, b). rolandique) is lightly marked in Guercy 1. The sulcus
In general, the degree of lateral expansion of the STG deepens and widens dorsally such that the dorsal portion
coupled with a greater or lesser degree of inflation of the of the prcs can be followed as it diverges dorsocaudally
frontoparietal operculum tends to either demarcate or from the imprint of the coronal suture (Figure 1b, c). The
obscure the position of the ls. In the Sima de los Huesos ability to discern the course of the prcs in Guercy 1 is, in
Preneanderthals, the dorsal aspect of the STG is uncov- part, aided by the rostral position of the superior aspect
ered by a lack of development of the frontoparietal oper- of the coronal suture, as discussed in Richards et al.
culum and parietal lobe, generally. This disjunction is (2021). The dorsal prcs terminates in the sfs-p. In
readily apparent in a superior view of the Sima de los Ehringsdorf H, the dorsal portion of the prcs is identified
Huesos endocasts (cf. SH-4: Poza-Rey et al., 2019). In by Grimaud-Hervé (1997) as being prolonged into the
Guercy 1, the frontoparietal operculum is laterally devel- midsagittal region in direct association with the impres-
oped such that the bi-temporal lobe breadth is exceeded. sions for the “great anterior vein” (sensu Trolard, 1890)
This results in the ls becoming more linear and discrete, and middle meningeal neurovascular bundle. This rela-
with less of an offset between its dorsal and ventral bor- tionship is like that in Guercy 1, with the exception that
ders. In the Early Neanderthal Apidima 2, the left STG Guercy 1 lacks an impression for a great anterior vein. In
extends laterally to a greater degree than the frontoparie- the Le Ferrassie 1 Late Neanderthal, a sulcus identified
tal operculum, such that a wide impression is present dor- by Heim (1970) as the prcs is well rostral of its usual posi-
sal to the STG (de Lumley et al., 2020; Guipert tion caudal to the coronal suture. There is, however, a
et al., 2019). On the right side, however, the frontoparietal second sulcus which is positioned slightly more caudally
operculum more closely approximates the lateral expan- that is more consistent with the position of the prcs.
sion of the STG. A similar bilateral difference is also pre- Anthony (1913) discusses a similar situation in his
sent in the Sima de los Huesos Preneanderthal endocasts. description of La Quina H5 wherein there is a sulcus
Bilateral asymmetry in the ls also occurs in recent positioned rostral to the coronal suture. He concluded
humans and is attributed to Yakovlevian troque, possibly that it is not the prcs. More recently, Grimaud-Hervé
related to handedness (Toledo et al., 2021). Taking both (1997) has identified the location of the prcs in
sides of Apidima 2 into account, the degree of develop- Ehringsdorf H, Feldhofer 1, Devil's Tower 1, La Chapelle-
ment of the ventrolateral parietal lobe is like that in aux-Saints 1, and Le Moustier 1. Her work confirms
Guercy 1, although its most lateral extent is slightly more Anthony's (1913) observation that the dorsal prcs is posi-
inferiorly placed. Saccopastore 1 differs from both Guercy tioned near, or caudal to, the coronal suture and that it
1 and Apidima 2, as the ls is not clearly visible (Bruner & associates with the anterior ramus of the middle menin-
Manzi, 2008), and the region of the parietal lobe compris- geal neurovascular bundle.
ing the supramarginal gyrus (SMG) and angular gyrus In Guercy 1, the PrCG is developed in its medial
(AnG) is more expanded. This morphological difference region but not well marked ventrally or dorsally. This
fills in the gap superior to the ls and makes Saccopastore developed region appears to be related to a dorsoventrally
1 more like Late Neanderthals. Further discussion of this disposed gyral extension that joins the MFG with the
difference can be found both below and in the description PrCG, thereby dividing the sulcus into ventral and dorsal
of the ectocranial morphology (Richards et al., 2021). portions, as in some modern humans (Petrides &
Although standard anatomical orientations cannot be Pandya, 2012). The PrCG lies rostral to the ventral por-
utilized for Guercy 1 due to missing cranial regions, the tions of the anterior ramus of the middle meningeal neu-
course of the ls appears nearly horizontal as in Apidima rovascular bundle. In Apidima 2, the region of the PrCG
2, Krapina 6, and Saccopastore 1 (Figure 1a). The hori- is damaged but is consistent with the morphology of
zontal nature of the Neanderthal ls was noted by Heim Guercy 1. The PrCG is also not well marked in Saccopas-
(1976) during description of La Ferrassie 1, based in part tore 1 likely due, in part, to the laterally directed expan-
on the endocranial anatomy and sulcal orientation in La sion of the SMG and AnG. In the Late Neanderthals La
Quina H5. However, the orientation of the ls in La Chapelle-aux-Saints 1 and La Ferrassie 1, the PrCG is vis-
Chapelle-aux-Saints 1 is more horizontal than in La Fer- ible with a distinct swelling of its medial region as in
rassie 1, and both are less horizontal than in the early Guercy 1, but the extent of the swollen region is greater.
group (cf. Guercy 1, Apidima 2, Krapina 6, Saccopastore The central sulcus (cs) is clearly visible on the Guercy
1). This difference in sulcal angulation is likely driven by 1 endocast, and it can be followed from its ventral extent,
576 RICHARDS ET AL.
dorsal to the ls, as a wide and caudodorsally arcing Ferrassie 1 > La Chapelle-aux-Saints 1). In this case, the
impression that terminates near the vertex (Figure 1a–c). result is a caudally directed midline extension of the
Large parasagittally placed lateral lacunae delineate its expanded SFG and parietal lobe such that the caudoven-
dorsal-most extent on the parietals (Figure 1a–c). A simi- tral slope of the midsagittal parietal is moved caudally.
lar demarcating relationship between the lateral lacunae An exception to this morphology occurs in La Quina H5,
and the prcs and cs has been noted in Neanderthals, in as it lacks inflation of the midsagittal portion of the ros-
general, by Grimaud-Hervé (1997). tral parietal lobe, being in this case more like Guercy 1.
The relationship of the cs to the coronal suture in Just caudal to the PoCG a widened portion of the
Guercy 1 appears to differ from those Neanderthals in inferior postcentral sulcus (pocs) demarcates the rostral
which the cs has been identified and from recent edge of the superior marginal gyrus (SMG; Figure 1a–c),
humans. Such a difference would, however, be unex- a portion of the inferior parietal lobule (IPL). The pocs is
pected based on the findings of Cunningham (1892), who visible along its ventral and dorsal-most extents, but it is
observed a remarkably consistent relationship between not preserved centrally. Where the ventral end of the
these two structures in recent humans. The perceived inferior pocs becomes co-incident with the ls, the parietal
caudal placement of the cs relative to the coronal suture lobe is not well developed in Guercy 1. This results in a
in Guercy 1 is likely a result of the frontal bone lacking a depressed region of the parietal lobe in the area where
normal caudally directed extension medial to the tempo- the pocs wraps around the ventral aspect of the rostral-
ral lines (Figure 1: Richards et al., 2021). In support of most SMG (Figure 1a–c). A portion of this depressed
this view, the prcs, PrCG, cs, and middle meningeal neu- region may correspond to a supramarginal sulcus, a
rovascular grooves in Guercy 1 have a normal relation- structure that is variably present in recent humans
ship for Early Neanderthals. However, the distance from (Petrides, 2013). This ventral region of the parietal lobe,
bregma to the cs in Guercy 1 is ≈46 mm, a distance con- comprising the subcentral gyrus (=base of central sulcus)
sistent with that provided by Anthony (1913) for La and rostroventral most aspect of the SMG, is not as later-
Quina H5 (≈44 mm) and by de Lumley (1973) for Lazaret ally placed as the rostral aspect of the superior temporal
1 (≈45 mm), the Cova Negra parietal I (≈47 mm), and gyrus (STG: Figure 1b). In Preneanderthals, a similar
recent humans (≈48 mm). These data indicate that the morphology is present in some of the Sima de los Huesos
suture is maintaining a reasonably close relationship to individuals (cf. SH-3, SH-5: Poza-Rey et al., 2019) and
the cs and middle meningeal neurovascular bundle even Swanscombe 1 (left side: Keith, 1938). In Early Neander-
though the frontal squama is foreshortened. thals, Apidima 2 (de Lumley et al., 2020; Guipert
Caudal to the cs, the postcentral gyrus (PoCG) is visi- et al., 2019), Biache-Saint-Vaast 1 (Grimaud-Hervé, 1997)
ble and overlain by a branch of the anterior ramus of the and Krapina 3 and 6 are like Guercy 1, while Saccopas-
middle meningeal neurovascular bundle (Figure 1a–c). tore 1 is more developed in this region. In the Late Nean-
Near its dorsal-most extent, this gyrus is not visible on derthal La Ferrassie 1, the parietal lobe is developed and
the endocast, which appears flat and ventrocaudally lacks clear depressions rostroventral to the pocs and
retreating in this region. In the Sima de los Huesos Pre- SMG. Alternatively, La Chapelle-aux-Saints 1 shows
neanderthals the PoCG tends to flatten as the midsagittal some development caudal to the pocs, but the region of
region is reached, as in Guercy 1. However, instead of the the parietal lobe dorsal to the ls and ringing the ventral
superior parietal lobule (SPL) flattening caudal to the aspect of the SMG is depressed. Endocasts of Cro Magnon
PoCG, as in Guercy 1, it is variably inflated in the Sima 1 (Balzeau et al., 2012), Cioclovina 1 (Kranioti
de los Huesos specimens (cf. SH-2 vs. SH-13). The mor- et al., 2011), Předmosti 3, 4, and 9 (Holloway et al., 2004),
phology of this region in Preneanderthals appears as an and recent humans have more developed gyri in this
expansion along the midline, resulting in the observed region and, therefore, lack these depressed regions. Such
midsagittal peaking and longitudinal parasagittal depres- expansion appears to be related to a greater development
sions. A pattern like Guercy 1 can be observed in Sacco- of this portion of the frontoparietal operculum and differ-
pastore 1 (Bruner & Manzi, 2008) and Apidima ences between Neanderthals and H. sapiens in position-
2 (de Lumley et al., 2020). In Early Neanderthals, the lack ing of the neural mass relative to the cranial base.
of development in this region results in a flat transition Expansion of the underlying insular gyri may also
from the frontal to the parietal lobe and a distinct caudo- explain, or contribute to, the lateral projection of this por-
ventral slope to the midsagittal region (cf. Krapina 3, Sac- tion of the frontoparietal operculum.
copastore 1). In Late Neanderthals, the caudal SFG and Whereas the rostral portion of the SMG in Guercy
dorsal portion of the PoCG are expanded, but caudal to 1 appears as an isolated and developed region, its caudal
the PoCG the SPL is only minimally expanded at its ros- extent is more evenly developed relative to the surround-
tral extent, with the lobule flattening caudally (cf. La ing gyri. In this region, the SMG grades into a partially
RICHARDS ET AL. 577
preserved angular gyrus (AnG), which is similarly devel- and the region caudal to the coalescence of the AnG and
oped. In total, the combined SMG–AnG is relatively the second and third caudal branches of the STG, as well
poorly developed in Guercy 1 (Figure 1a–c). In the Sima as into the MTG and ITG. This coalescence is one of the
de los Huesos endocasts, development of this region of factors that results in a reduction in the angularity of
the inferior parietal lobule varies (SH-3, SH-9 discrete the mid-parietal lobe and a ventrolateral displacement of
and expanded; SH-4, SH-5, SH-11 expanded but less dis- the temporal squama.
crete; SH-6 less discrete and less expanded). While vari- In Guercy 1, the region extending around the ventral
able, the mid-parietal lobe in all the latter crania is aspect of the AnG is concave, weakly developed, and is a
relatively expanded and, when combined with the rostral continuation of a slightly depressed region
expanded temporal lobe, is associated with a lateral pro- between the STG and MTG (Figure 1b). A similar mor-
trusion of the cranial wall, as described by Arsuaga et al. phology is also seen in the Preneanderthal SH-3. In Early
(1997). This lateral development results in a widening of Neanderthals, Apidima 2 is like Guercy 1 except that the
the generally oval shape of the endocranial outline. ventral portion of the AnG appears less developed. Note,
Although only partially preserved in Apidima 2, the gyri however, that in Apidima 2 the region just caudal to the
in this region are less developed relative to Prenean- cs differs from Guercy 1; it is less well-developed, and
derthals and Guercy 1. The weak projection of the left there is a greater decrease from the SMG to the AnG that
frontoparietal operculum leaves a depression dorsal to then continues into the region caudal to the AnG. Kra-
the ls, the dorsal border of which is not as laterally placed pina 6 is like both Guercy 1 and Apidima 2 in showing
as the STG. In contrast, the right frontoparietal opercu- reduced development caudal to the AnG. In Saccopastore
lum appears to extend over the ls to the lateral-most STG, 1, the region caudal to the AnG is a concave depression,
with the result being a more evenly curved lateral tem- but the concavity does not extend into the second and
poroparietal region. In Krapina 6, the right SMG–AnG is third caudal branches of the STG as it does in Guercy
well developed and laterally expanded, and it overhangs 1 and Krapina 6. In contrast, in both La Chappelle-aux-
the STG. The ls is deep and wide, because the frontopar- Saints 1 and La Ferrassie 1, the SMG–AnG is a broad,
ietal operculum and STG are equally expanded laterally swollen region that merges with the caudal branches of
but have not become appressed. The region rostral to the the STG, although there is some depression of the region
AnG is less well developed. Further, the second and third caudal to the left AnG in La Chappelle-aux-Saints 1.
caudal branches of the STG form part of a distinct swell- Moving to the more dorsal region of this view, the
ing of the caudal temporoparietal, but the parietal is medial aspect of the parietal lobe caudal to the PoCG in
much less developed caudal to this region, and this Guercy 1 is not well marked by individual portions of the
results in a very discrete caudal border to the swelling. SPL (Figure 1b, c). However, the caudal extent of the SPL
The discrete nature of this region in Krapina 6 is similar is visible and aligns with the dorsal-most extent of the
to, but more developed than, that in the Sima de los Hue- IPL, as in other Neanderthals. A similar lack of morpho-
sos Preneanderthals. In Krapina 3, the SMG–AnG and logical detail characterizes Swanscombe 1 (Le Gros
second and third caudal branches of the STG are more Clark, 1964b), Saccopastore 1 (Bruner & Manzi, 2008), La
like the condition in Guercy 1. The region forms a dis- Chapelle-aux-Saints 1, and La Ferrassie 1. Although por-
crete swelling that lacks the sharp caudal boundary seen tions of the IPL are missing in Guercy 1, its dorsal extent
in Krapina 6. In Saccopastore 1, the SMG–AnG region is preserved and is morphologically like Lazaret
appears as a discrete swelling caudal to the PoCG that 1 (de Lumley, 1973: Figure 1a–c). The preserved Guercy
involves the SMG, AnG, and second and third caudal 1 IPL is well delineated dorsocaudally by a narrow,
branches of the STG. Where Saccopastore 1 differs from superficial interparietal sulcus. The rostral portion of the
Apidima 2, Guercy 1, and Krapina 3 and 6 is that the interparietal sulcus is missing, but the preserved extent
more dorsal aspects of the IPL are more developed. This shows it to arc around the IPL and course rostroventrally
results in a diffuse swelling with a clear shelving of the toward the PoCG. The configuration of the interparietal
parietal along the dorsal border of the IPL. This morphol- sulcus in Guercy 1 is like Sima de los Huesos SH-3 and
ogy is more like that seen in the Late Neanderthals, SH-6. In the region dorsal to and including the interpar-
although in Saccopastore 1 the region caudal to the AnG ietal sulcus, the morphology of Reilingen 1 (Dean
is less inflated, which is also characteristic of Guercy et al., 1998) is like that of the Sima de los Huesos Pre-
1 and other Early Neanderthals. In the Late Neanderthals neanderthals by being depressed between the SPL and
La Chapelle-aux-Saints 1 and La Ferrassie 1, the dorsal IPL. However, Reilingen 1 and Guercy 1 share the posi-
part of the IPL is even more developed. Expansion of this tioning and shape of the interparietal sulcus and the gen-
region extends into the caudal aspects of the AnG (=pos- eral curvature of the lateral parietal lobe. The
terior inferior parietal and inferior parieto-occipital gyri) interparietal sulcus and SPL morphology of Saccopastore
578 RICHARDS ET AL.
1 are like those of Guercy 1. In Late Neanderthals (cf. La observed by Kappers (1936), the relatively flat frontal lobe
Chapelle-aux-Saints 1, Boule & Anthony, 1911; La Fer- of Ehringsdorf H rises steeply to create a peaked frontal-
rassie 1, Heim, 1970), both the IPL and SPL are more to-parietal lobe transition. This morphology is more like
prominent, and the interparietal sulcus is mediolaterally that of the Late Neanderthals. In La Chapelle-aux-Saints
broader. Further, the positioning of the dorsal-most arc 1, the midsagittal curvature of the frontal and parietal
of the IPL in Guercy 1 approximates the position of the lobes is relatively flat, but the height rises continuously to
maximum biparietal lobe breadth, as in these Late Nean- ≈30 mm posterior to bregma, whereafter it decreases to
derthals. This relationship was noted by Le Gros Clark create a relatively open angle as it approximates the occip-
(1964b) in Swanscombe 1 and associated by him with the ital lobe. La Ferrassie 1 is morphologically similar, with
positioning of the parietal eminence. However, where the exceptions that the frontal and parietal lobes are more
Guercy 1 and Late Neanderthals differ is that the dorsal steeply angled at the vertex and the caudal portion of the
extent of the IPL is more caudally positioned in Late frontal-to-parietal-lobe curvature is less flat than in La
Neanderthals, resulting in a more caudally positioned Chapelle-aux-Saints 1 (Figure 2b, c). In lateral view, Spy I
maximum breadth of the parietal lobes. The morphologi- and II share the same basic profile seen in these other
cal pattern observed in these parietal lobe regions in Late Neanderthals. However, compared with Spy I, Spy II
Guercy 1 is most like that expressed in Preneanderthals shows less frontal-to-parietal-lobe peaking and flattening
and in Early Neanderthals. as the occipital lobe is approximated (Thoma, 1975). As
discussed above, this morphological pattern in Late Nean-
derthals appears to be related to expansion of the medial-
3.4 | Frontoparietal curvatures most PoCG and rostral aspect of the SPL. An exception to
this Late Neanderthal pattern is seen in La Quina H5,
In lateral view, the rostrocaudal curvature of the frontal which lacks the stronger angulation between the frontal
lobe in Guercy 1 is relatively flat rostral to the coronal and parietal lobes (Kappers, 1936), making it more like
suture, with a slight convexity as it nears the rostral Guercy 1 and other Early Neanderthals.
extent of the preserved frontal lobe (Figure 1a). In the In superior view, the endocast of Guercy 1 has a slight
Sima de los Huesos Preneanderthals, the rostrocaudal rostrocaudal concavity at the junction of the fronto-
curvature of the frontal lobe varies, but it is generally orbital, temporal, and frontoparietal opercula (Figure 1c).
more steeply curved. This is also the case for Apidima This region is more concave in smaller-brained Homo
2. Frontal lobe curvature in Guercy 1 is most like Krapina (Grimaud-Hervé, 1997), and shallowing of this depressed
3 and Saccopastore 1, although it was still likely less region is characteristic of both Neanderthals and
curved at its rostral extent. H. sapiens (Bruner & Manzi, 2008). In Guercy 1, Apidima
Frontal lobe flatness can be further assessed by its 2, Biache-Saint-Vaast 2, and Ehringsdorf H, this region
height; however, a standard height dimension for the forms a distinct but shallow concavity. Variation among
frontal lobe cannot be measured on Guercy 1 due to dam- these Early Neanderthals relates to whether the parietal
age. Instead, assessing its height at approximately one- lobe is more expanded in the region just caudal to the cs,
third of frontal lobe length (sensu Bruner & Manzi, 2008) making the concavity less shallow as in Apidima
produces a height of ≈50 mm. The values for Saccopas- 2 (Guipert et al., 2019), or less expanded, making the con-
tore 1 and Salé provided by Bruner and Manzi (2008) are cavity shallower as in Guercy 1. Expansion of the under-
51 and 50 mm, respectively. These authors' mean frontal lying insula, or a combined development of the two
lobe height for Late Neanderthals is 58 mm. The differ- regions, may also account for the infilling of this region.
ence in frontal lobe height between these Early and Late In the Sima de los Huesos Preneanderthals, the concavity
Neanderthals is reflected in the more dorsally expanded of this region varies, but in those individuals lacking
rostral portion of the frontal lobe and a more acute more extensive mid-parietal lobe expansion, this region is
frontal-to-parietal-lobe angle in lateral view in Late most like Guercy 1 and other Early Neanderthals. In the
Neanderthals. This difference is related to a greater Late Neanderthals, the concavity shallows and broadens,
expansion of the prefrontal (Parks & Smaers, 2018) and with La Chapelle-aux-Saints 1 and Feldhofer 1 being
premotor cortex in the late group (Figure 2c). shallower than La Ferrassie 1 (Figures 2b, c and 3b, c).
The combined curvature of the frontal and parietal As discussed above, shallowing of this region in the late
lobes of Guercy 1, in lateral view, is nearly identical to group results, in part, from their greater development of
Krapina 3 and Saccopastore 1 (Bruner & Manzi, 2008). In the IFG–ventrolateral MFG, inclusive of the Broca's cap.
all three cases, the frontal and parietal lobes form a low, This expansion of the frontal lobe is coupled with a
flat arc until mid-parietal, whereafter they descend at a greater development of the middle-to-caudal portion of
steep angle toward the occipital region (Figure 2b). As the frontoparietal operculum, the PrCG, and the PoCG.
RICHARDS ET AL. 579
F I G U R E 4 (a–c) Graphs depicting the relationship between (a) the maximum breadth between the Broca's caps and the maximum
frontal lobe breadth; (b) the maximum frontal lobe breadth and the maximum endocast breadth; and (c) the maximum breadth between the
Broca's caps and the maximum endocranial breadth. The Preneanderthals from Sima de los Huesos (Atapuerca) are denoted as SH
3.5 | Frontal and parietal lobe metrics variation in this group (Figure 4, Tables 3 and S2). Sacco-
pastore 1 falls in the extreme upper end of the Prenean-
Assessment of the maximum breadth between Broca's derthal range (Tables 3 and S2 and Figure 4c). Relative to
caps shows that the Guercy 1, Apidima 2, and Ehrings- Late Neanderthals, Saccopastore 1 shares a breadth value
dorf H breadths are significantly greater (p < .001) than with La Quina H5, falling into the lowest end of the
the Preneanderthal mean and do not overlap the range of range. Alternatively, the breadth between the Broca's
580 RICHARDS ET AL.
T A B L E 3 Endocast breadths (in mm) for Preneanderthals, variation of Preneanderthals but lies below the ranges of
early Neanderthals, late Neanderthals, and upper Paleolithic and Early and Late Neanderthals. Comparing the maximum
recent Homo sapiensa breadth at the Broca's caps to that of the frontal lobe
Maximum Maximum shows that the Preneanderthals, Late Neanderthals, and
breadth at frontal Maximum Ehringsdorf H lie within the distribution for the H.s.
Broca's lobe breadth of group. Guercy 1 and Apidima 2 (Figure 4, Tables 3, and
capsb breadthb endocastb S2) both fall outside the distribution due to their wide
Guercy 1 (114.2)c (116.0)c (138.0)c maximum breadths at the Broca's cap relative to their
Preneanderthals maximum frontal lobe breadths. The Upper Paleolithic
N 15 16 18 H.s. group lies near the upper edge of the distribution,
Range 88.7–103.3 103.8–122.3 126.8–146.6 but in this case, it is because they have wide maximum
frontal lobe breadths relative to their maximum Broca's
x 96.9 111.3 134.8
cap breadths.
SD 4.053 5.067 5.158
Considering the maximum breadth of the endocast,
Early Neanderthals Guercy 1, Apidima 2, and Krapina 3 share the greatest
N 3 2 5 maximum endocast breadths for Early Neanderthals
Range 102–114.8 119.3–121 131–139 (Table S2). In Preneanderthals, the maximum endocast
x 108.3 135.4 breadth occurs in the temporal region and, while their
mean breadth is narrower, Guercy 1 falls within the
SD 6.40 3.21
range of variation for this group (Table 3; Poza-Rey
Late Neanderthals
et al., 2019). Although the dorsoventral positioning of the
N 6 5 10 widest point varies slightly in Early Neanderthals, its
Range 102–115 118–127 131–150 positioning has moved dorsally to the temporoparietal
x 111 122.6 141 junction, as in Guercy 1. This similarity suggests that a
SD 5.24 4.037 5.73 greater development of the frontoparietal operculum in
Neanderthals (Early and Late) Early Neanderthals is driving at least a portion of the
morphological differences between the Preneanderthal
N 8 6 13
and Early Neanderthal endocasts. In Late Neanderthals,
Range 102–115 118–127 131–150
the mid-temporal region is expanded, as occurs in Early
x 110 122.3 139.3 Neanderthals, but this is accompanied by expansion of
SD 5.45 3.67 5.68 the caudal parietal and temporal lobes (=SMG, AnG, sec-
Upper paleolithic Homo sapiens ond and third caudal branches of the STG), resulting in
N 4 6 5 the maximum breadth shifting caudally (Figure 2c).
While there is some overlap, comparing the mean maxi-
Range 105–117 122–137 132–146
mum endocranial breadth values for the Early and Late
x 110.3 127.7 138.5
Neanderthals shows the Late group to be significantly
SD 4.99 5.16 5.28 broader (p < .001) than the Early group.
Recent Homo sapiens Comparing the maximum breadth at the Broca's caps
N 45 45 45 with the maximum endocast breadth shows Guercy
Range 99–123 106–140 120–154 1, Apidima 2, Ehringsdorf H, and Saccopastore 1 to plot
x 107.8 120.5 135 along a line at the lower edge of the distribution. This is
due to their narrow maximum endocast breadths relative
SD 6.15 7.83 8.47
to their maximum Broca's cap breadths (Figure 4c). Bru-
a
The composition of each group, metric values by specimen, and references ner et al. (2006) discuss the relationship between the
for the metric data can be found in the Supplemental Data, Table S2.
b maximum breadth at the Broca's caps and the maximum
Measures are defined in Poza-Rey (2015).
c
Measures in () are estimates. Values for Guercy 1 derive from a virtual endocast breadth for Krapina 3 and 6; however, they do
endocast that was made following reconstruction and mirror-imaging of the not provide metric values, and Krapina 6 does not pre-
preserved cranial fragments, as described in Richards et al. (2021). serve the right Broca's cap. Putting aside these issues, the
graphs in Bruner et al. (2006) indicate that Krapina 3 and
6 would plot within our Preneanderthal cluster along
caps in Guercy 1, Apidima 2, and Ehringsdorf H lies near with Saccopastore 1. The Late Neanderthals Feldhofer
the mean for the Late group. Considering the maximum 1, Ganovce 1, La Quina H5, and Teshik Tash 1 plot with
frontal lobe breadth, Guercy 1 falls within the range of the Early Neanderthals, while La Chapelle-aux-Saints
RICHARDS ET AL. 581
Poza-Rey, 2015; Poza-Rey et al., 2019). Alternatively, in

Late Neanderthals (=La Chapelle-aux-Saints 1, La Fer-
rassie 1, La Quina H5, Le Moustier 1; x = 181.4, 177.5–
183 mm, N = 4, Poza-Rey, 2015) the maximum endocra-
nial length is greater, and all the earlier material falls
below the range of variation for this group.
3.6 | Endocranial neurovascular grooves

and sinuses
F I G U R E 5 Configuration of the left middle meningeal
neurovascular bundle in Guercy 1. Note the anterior dominance of Impressions associated with the left middle meningeal
the pattern with the anterior (ArMA) and middle ramus (MrMA) neurovascular bundle are the most complete and do not
providing the major portion of the blood supply. The posterior differ substantially from the right side. Three main rami
ramus (PrMA) is only represented by a short, non-bifurcated are present, but the point of bifurcation of the anterior
segment. Bifurcations of the main rami are denoted as primary (1 ),
and middle rami is not preserved (Figure 5). The
secondary (2 ), and tertiary (3 ). The impressions are consistent
rostral-most primary ramus initially lies over the PoCG
with Adachi's (1928) Type I pattern
and approaches the pocs. A secondary division of this
ramus gives rise to three tertiary branches. The most
1 and La Ferrassie 1 have especially wide maximum rostral of these branches continues dorsally to lateral
endocast breadths relative to their maximum Broca's cap lacunae in the bregmatic region. A final terminal
breadths (Figure 4c). The Upper Paleolithic H.s. branch arises just before the neurovascular bundle
Předmosti X and Cro-Magnon 3 both fall within the mid- reaches the lacunae. The other two tertiary branches
dle of the Preneanderthal–Late Neanderthal and modern from the secondary branch of the anterior ramus are
H.s. cluster. only partially preserved, but the middle tertiary branch
Assessment of the relationship between the maxi- is bifurcated. These two tertiary branches supply the
mum breadth of the frontal lobe and that of the parietal region from the cs to the SPL and interparietal sulcus
lobes (=maximum endocast breadth) shows Guercy (Figures 1c and 5).
1, Apidima 2, and Ehringsdorf H to all lie within the Thin terminal branches (≤0.5 mm) arise from the ros-
upper end of the Preneanderthal cluster (Figure 4b). Con- tral edge of the anterior ramus, extending to but not across
sidering the Late Neanderthals, Feldhofer 1 plots near the coronal suture (Figure 5). Numerous small vascular
Guercy 1 and Apidima 2 while La Quina H5 lies deeper foramina are present along the suture and around these ves-
within but on the lower edge of the Preneanderthal clus- sels. Similar foramina are present in our juvenile human
ter. Other Late Neanderthals have greater maximum sample, perhaps associated with active sutural growth. Sim-
frontal and endocast breadths relative to the Early Nean- ilar, but shorter, fine and transversely oriented grooves orig-
derthals. The Upper Paleolithic H.s. group plots with the inating from the anterior ramus are also seen in some
Late Neanderthals but tends to have narrower maximum Preneanderthals (cf. Arago 47: Holloway et al., 2004; SH-13
endocast breadths relative to their maximum frontal lobe and 14: Poza-Rey, 2015), Early Neanderthals (cf. Krapina 6:
breadths (Figure 4b). Cro-Magnon 3 differs from this Holloway et al., 2004; Saccopastore 1: Bruner &
trend as it plots with those Late Neanderthals Manzi, 2008), and Late Neanderthals (cf. Engis 2, Feldhofer
(La Chapelle-aux-Saints 1 and La Ferrassie 1) having the 1, La Quina H5, La Chapelle-aux-Saints 1, Le Ferrassie
widest maximum endocast breadths. Dolni Vĕstonice II is 1, Le Moustier 1). Our ontogenetic sample of recent
an outlier in the Upper Paleolithic group, with both a H. sapiens (5–8.0 years) shows that grooves for these
very narrow maximum endocast and frontal lobe branches are short and wide (≈0.5–1.0 mm) in 52–59% of
breadth, being in this case, like La Quina H5. individuals, with the remainder having linear and longer
The maximum length of the Guercy 1 endocast can- impressions or longer impressions on the frontal that arc
not be determined but, given the preserved portions, it back to form an anastomosis between two short branches
was likely greater than Saccopastore 1 (161 mm; (Cronin et al., 2022). With age increase, these small
Bruner & Manzi, 2008), being most like Ehringsdorf H branches are considered to increase in diameter and extend
(174 mm: Kappers, 1936). The Early/Late Neanderthal onto the frontal (Saban, 1995). Given the variation observed
Gibraltar 1 has a maximum length of 167 mm. Both the by Cronin et al. (2022), however, it appears that, if these
Early Neanderthals and Gibraltar 1 fall within the Pre- middle meningeal neurovascular vessels do extend onto the
neanderthal range (x = 165.9, 159–174.4 mm, N = 12, frontal lobe with age increase, there is high idiosyncratic
582 RICHARDS ET AL.
variation in the timing of any extension and potential anas- neurovascular bundle (Figures 1c and 5). In the Krapina
tomoses with other such branches. 1 juvenile, Minugh-Purvis et al. (2000) describe an
The middle ramus arises from the anterior ramus as a impression that overlaps the course of the anterior ramus
primary bifurcation in Guercy 1. One branch supplies the of the middle meningeal artery and that merges into the
SMG–AnG region. The other branch follows the course “sinus of Breschet”. In the Ehringsdorf H Early Neander-
of the ls, generating a terminal branch that anastomoses thal, both Vlček (1993) and Grimaud-Hervé (1997) sug-
with the posterior ramus (Figure 5). The posterior ramus gest that an impression for an enlarged anterior
appears to have arisen from the main trunk near the fora- meningeal vein is present. Sarri on (2006) and Arsuaga
men spinosum, but this region is not preserved. This iso- et al. (2012) suggest that an enlarged impression on the
lated ramus likely traversed the petrosquamous junction/ Bolomor Cave parietal (HCB-07) represents a sphenopar-
parietal notch to reach the ventrolateral aspect of the pos- ietal, or Breschet's, sinus. In Preneanderthals, Poza-Rey
terior parietal lobe (Figure 5). (2015) suggests that an impression for an enlarged vein
The distribution of the middle meningeal neurovascu- occurs in 40–50%, of the Sima de los Huesos crania, and
lar bundle in Guercy 1 has a sub-vertical course, is domi- Grimaud-Hervé (1997) suggests that such an impression
nated by branches from the anterior ramus, lacks is also present in Swanscombe 1.
substantial arborization, and can be classified as a Type I In Guercy 1 the superior sagittal sinus reaches a maxi-
pattern (sensu Adachi, 1928). Krapina 6 is like the pat- mum width of 4.2 mm rostrally (Figure 1b, c). On the left
tern in Guercy 1, with a Type I classification (Bruner side, the sulcus is marked by a prominent lateral ridge.
et al., 2006) and dominance of the anterior ramus, but it On the right side, the lateral ridge fades into the squama
has more arborization. In the Krapina 1 juvenile, the at ≈11 mm rostral to the coronal suture as it gives way to
meningeal system is anteriorly dominated and appears to an expansive lateral lacuna in the bregmatic region
have a Type I pattern (Minugh-Purvis et al., 2000). (≈28 16 mm, Figure 1b, c). This expanded lacuna is
Although the complete meningeal pattern is obscured in likely related to a left side deviation in the first section of
Ehringsdorf H, Grimaud-Hervé (1997) suggests that it the sagittal suture. From the frontal venous lacuna, the
was anteriorly dominated, as in Krapina 6 and Guercy superior sagittal sinus is ill-defined until it transitions
1. Biache-Saint-Vaast 2 and Saccopastore 1 have simple, into large parietal lateral lacunae (≈23 16 mm,
posteriorly dominated Type II patterns, while Krapina Figure 1b, c). Posterior to the parietal lacunae, the supe-
3 has a Type III pattern, being supplied by both the anterior sagittal sinus is again marked by lateral ridges on the
rior and posterior rami (Bruner et al., 2006; Bruner & preserved right side. The large lateral lacunae are associ-
Manzi, 2008). The Bolomor Cave HCB-07 parietal has a ated with variably sized arachnoid foveae.
simple pattern with fine ramifications that lack extensive
anastomoses (Arsuaga et al., 2012; Sarri on, 2006) but is
not assigned to a type. 4 | DISCUSSION
The middle meningeal neurovascular bundle nor-
mally comprises an artery and three small veins, in addi- Chronostratigraphic and biostratigraphic evidence asso-
tion to nerves (Ruïz et al., 2004; Tubbs et al., 2007). In ciate the Neanderthal skeletal remains from Baume
some cases, one or more impressions that are considered Moula-Guercy with the Last Interglacial (MIS 5e). Fur-
to represent hypertrophied veins(?) are visible on the ther, recent ontogenetically based assessments of the
endocranial surface and these connect the superior sagit- cranial sample have demonstrated that these remains
tal sinus and anterior venous lacuna with the middle possess ectocranial features consistent with those
meningeal system. In Neanderthals, an impression for a observed in MIS 7–MIS 5e associated Early Neander-
hypertrophied vessel has been suggested to be present in thals (Richards et al., 2021, 2022). When the endocranial
many specimens (cf. La Chapelle-aux-Saints 1, La Ferras- anatomy of Guercy 1 is considered, however, the assess-
sie 1, La Quina H5, Feldhofer 1: Boule & Anthony, 1911; ment is hampered by the small sample of Early Nean-
Anthony, 1913; Heim, 1970; Saban, 2007), where it is var- derthal endocasts (N = 10, Table 1). Saccopastore 1 is
iously referred to as the “sphenoparietal sinus” (sensu the only relatively complete specimen, and three of the
Breschet) or as the “great anterior vein” (Trolard, 1890). other individuals are represented by a single cranial
Note, however, that these terms are not synonymous. bone each (Bolomor HCB-07: Sarri on, 2006; Arsuaga
Guercy 1, Saccopastore 1 (Bruner & Manzi, 2008), et al., 2012; Lazaret 1 and 24: de Lumley &
Krapina 3 and 6 (Bruner et al., 2006), and Apidima 2 all Piveteau, 1969; de Lumley, 2018). However, even given
lack evidence of an impression for an enlarged vein run- this limitation, we describe features of the Guercy
ning from the sagittal sinus or lateral lacunae, either sep- 1 endocast that augment a morphological connection to
arately or as one component of the middle meningeal the Early Neanderthal chronostratigraphic group and
RICHARDS ET AL. 583
further differentiate this group from both Prenean- and Late Neanderthals. Late Neanderthal endocranial
derthals and Late Neanderthals. shape generally differs from the Preneanderthal–Early
Neanderthal condition in having a more angular outline
in superior view (Figure 2b). The shape change is driven
4.1 | Guercy 1 and the evolution of the by a posteriorly dominated widening of the frontal lobe
Preneanderthal–Neanderthal (Bruner & Holloway, 2010) that results in a more V-
Endocranium shaped frontal lobe in superior view. This change is
coupled with an expansion of the caudal parietal and
Guercy 1 and other Early Neanderthals differ from Pre- temporal lobes, with the result being posteriorly diverg-
neanderthals in a series of features of endocast shape and ing lateral walls of the endocast in superior view
morphology in superior view. Most of their endocasts (Figure 2b). This relationship varies, however, with La
have a more rounded-oval shape (Figure 2). This com- Chapelle-aux-Saints 1 and La Ferrassie 1 showing espe-
pares to a wide-oval shape in Preneanderthals that is cially great biparietal breadths. This shape differs from
driven by the widest point of the endocast being in the the more parallel lateral walls of the Early Neanderthal
temporal region and their having relatively narrow fron- endocast, as seen in Guercy 1. Further, these changes
tal lobes, relative to Early Neanderthals. The more result in a sharper angle between the lateral wall and
rounded shape of Early Neanderthals is associated with the caudal endocast, as well as a shorter caudal region,
an increase in the width of the prefrontal and premotor unlike the longer convexity of the caudal endocast that
cortex relative to that observed in Preneanderthals. Fur- is present in Apidima 2, Saccopastore 1, and, given the
ther, in Early Neanderthals, the development of these preserved regions, Guercy 1. The expanded SFG,
regions combines with expansion of the rostral-to-middle medial-most PoCG, and rostral-to-middle SPL in Late
frontoparietal operculum to reduce the depth of the con- Neanderthals results in a swollen region that extends
cavity of the PrCG-to-PoCG region seen in Prenean- further posteriorly, relative to the Sima de los Huesos
derthals. Maximum breadth of the endocast is in a Preneanderthals and the Early Neanderthals. Expansion
similar position rostrocaudally in Preneanderthals and of these parasagittal structures in Late Neanderthals
Early Neanderthals, but in Preneanderthals it occurs at does not appear to result in a greater lateral extension
the STG, while it is at the IPL in Early Neanderthals such of the SPL, as both Guercy 1 and Apidima 2 are reason-
as Guercy 1. Saccopastore 1 differs from Guercy 1 and ably similar in the mediolateral distance from the mid-
other Early Neanderthals in having its maximum endo- line to the medial-most IPL. The difference, then,
cast breadth positioned slightly more caudally due to appears to be confined to an uplifting of the midsagittal
greater expansion of the dorsal aspect of the IPL and the frontoparietal that couples with greater lateral develop-
second and third caudal branches of the STG. Note, how- ment of the IPL and second and third caudal branches
ever, that the ectocrania of both Biache-Saint-Vaast of the STG to create the characteristic swelling of the
1 (Rougier, 2003) and La Chaise Bourgeois-Delaunay caudal temporoparietal region of Late Neanderthals.
17a-b (Condemi, 2001) have been described as having This medial swelling of the SPL and lateral expansion of
their maximum biparietal breadth in the caudal one- the IPL and second and third caudal branches of the
third, suggesting that their endocrania could be more like STG also accounts for the lack of parasagittal depres-
Saccopastore 1. However, Grimaud-Hervé (1997) con- sions and the greater dorsoventral curvature of the pari-
siders the maximum breadth of the endocast of Biache- etal lobes relative to those expressed in the Sima de los
Saint-Vaast 1 to be coincident with the SmG, making it Huesos Preneanderthals and, to a lesser degree, Early
like Guercy 1 and other Early Neanderthals. Compared Neanderthals.
with Preneanderthals, Guercy 1 has a wider frontal at the In a lateral view, the midsagittal region of the frontal
Broca's cap, as do other Early Neanderthals with the and parietal lobes in Guercy 1, Apidima 2, Krapina
exception of Saccopastore 1. Preneanderthals possess lon- 3, and Saccopastore 1 show a smooth but slight convexity
gitudinally oriented parasagittal depressions, which are without a distinct angular transition between the lobes
only weakly developed (Guercy 1 and Apidima 2) or (=peaking sensu Kappers, 1936). Although difficult to
absent (Saccopastore 1) in Early Neanderthals. In the measure due to fragmentation, Guercy 1, Apidima 2, Kra-
temporoparietal region, Guercy 1 and other Early Nean- pina 3, and Saccopastore 1 all share low frontal lobe
derthals have a more inflated SmG and AnG relative to heights. Further, in all these Early Neanderthals, the lack
Preneanderthals, resulting in slight dorsoventral round- of significant expansion of the SFG, medial-most PoCG,
ing of the parietal lobe. and SPL results in the midsagittal curvature rapidly
Guercy 1 superior endocast morphology also helps declining caudoventrally into the occipital lobe. The lack
clarify some differences between Early Neanderthals of expansion of these medially placed gyri results, in part,
584 RICHARDS ET AL.
in the reduced development or absence of parasagittal lobe of Late Neanderthals couple with changes between
frontoparietal depressions. the prcs and pocs to create a more open convexity of the
Although Guercy 1, Apidima 2, Ehringsdorf H, Kra- frontoparietal dorsal to the rostral-most ls. Further
pina 3, and Saccopastore 1 vary, they all have IFGs that changes involving the frontoparietal operculum, IPL, and
are not expanded relative to the MFG, and this translates the caudal branches of the temporal gyri result in a rela-
into frontal lobes that curve smoothly to the midsagittal tively discrete swelling of the ventrolateral parietal and
plane. Further, although the configuration of the pars temporal lobes, corresponding to a secondary parietal
opercularis, pars triangularis, and pars orbitalis varies eminence of the cranium (sensu Richards et al., 2021).
substantially (Keller et al., 2009;Poza-Rey, 2015; Poza- When compared with Late Neanderthals, the Sima de los
Rey et al., 2017, 2019), the pattern and degree of develop- Huesos Preneanderthals (Poza-Rey et al., 2019) and
ment in Guercy 1 is like that in the Sima de los Huesos Swanscombe 1 (Keith, 1938; Le Gros Clark, 1964b;
Preneanderthals (Poza-Rey, 2015; Poza-Rey et al., 2017, Marston, 1936) have a relatively low and variable swell-
2019) and other Early Neanderthals (Bruner & ing of the components comprising this neural region.
Manzi, 2008), while it differs from the greater develop- Referencing mainly the left hemisphere, this region fur-
ment of these IFG components in Late Neanderthals. The ther increases in area in the Early Neanderthals, espe-
region dorsal to the temporal lobe and approximating the cially Saccopastore 1. In Late Neanderthals, it is the
frontoparietal operculum in Early Neanderthals tends to development of the caudal aspect of the SPL–AnG, cau-
be less developed rostrally, and the region is generally dal branches of the temporal gyri, and the STG–MTG
depressed rostral to the SmG. The SmG and AnG are var- that are involved, in the main, in producing their charac-
iably developed relative to one another but, except for in teristic endocranial shape, as earlier suggested by Bruner,
Saccopastore 1, they are generally more developed rela- Amano, et al. (2018a); Bruner, Esteve-Altava, and
tive to the second and third caudal branches of the STG. Rasskin-Gutman (2018b); Bruner, Ogihara, and Tanabe
This places the region of maximum lateral expansion of (2018c). However, this expansion is not accompanied by
the parietal lobes in a similar position to Preneanderthals a major increase in the maximum endocranial breadth.
but rostral to that of Late Neanderthals. The potential The difference, then, appears to be one of an increase in
for a broader range of variation in positioning of the area, inclusive of the dorsal and caudal portions of the
maximum biparietal lobe breadth, as noted above parietal and temporal lobes (Bruner, Amano,
(Biache-Saint-Vaast 1, Rougier, 2003; La Chaise Bourgeois- et al., 2018a; Bruner, Esteve-Altava, & Rasskin-
Delaunay 17a-b, Condemi, 2001), requires further docu- Gutman, 2018b; Bruner, Ogihara, & Tanabe, 2018c).
mentation. In Guercy 1, Apidima 2, and Biache-Saint-Vaast Considering the range of variation in endocranial
2, the ventral PoCG, IPL, STG, and MTG comprise a rela- morphology in the Preneanderthal–Late Neanderthal
tively discrete lateral swelling of the temporoparietal. Sac- sequence, it appears that similar functional regions of the
copastore 1 is clearly more expanded in this region, brain are increasing in volume progressively. This appar-
particularly on the left hemisphere. The degree of neural ent lineal trajectory would lend some credence to the
development in this region in Early Neanderthals is greater accretion model of Neanderthal evolution (Dean
than that in Preneanderthals but less than that in Late et al., 1998; Hublin, 1998, 2000). However, such a conclu-
Neanderthals and is characteristic of this group. sion is true only in a limited sense, such as when one
When considered in lateral view, Late Neanderthals considers the prefrontal and premotor cortex as a whole.
(cf. La Chapelle-aux-Saints 1; La Ferrassie 1; Spy I and II) Note that we also see the same evolutionary changes in
have a variably distinct angle along the midsagittal plane the frontal lobe, and likely also the SmG and AnG, in the
between the frontal and parietal lobes. This increase in Homo sapiens group. Alternatively, by examining specific
height at the frontoparietal junction is partially related to neural regions, a more complex picture of localized gyral
expansion of the SFG, medial-most PoCG, and SPL. This expansion emerges, and this suggests a varying pattern of
angular change appears to result from a dorsocaudally emphasis on different functional regions. This is true of
directed expansion of the parietal lobes in Late Neander- the prefrontal and premotor cortex, as well as the parieto-
thals, as also discussed in Bruner (2004, 2014). The IFG is temporal region. While Preneanderthals and Early Nean-
more developed in Late Neanderthals, and this results in derthals are emphasizing similar portions of the
a slight bulging or step in the coronal profile of the fron- parietotemporal region, increases in Late Neanderthals
tal at the IFG and MFG. This set of changes in the frontal occur in the more caudal and dorsal aspects of the IPL
lobe results in a loss of the even convexity of the frontal and STG–MTG, and likely also the occipital lobe. As a
lobe in coronal section and an infilling of the slight con- result, the brain regions expanding in Late Neanderthals,
cavity of the prefrontal cortex seen in Preneanderthals which result in their characteristic cranial shape, are
and Early Neanderthals. These changes in the frontal topographically and, likely, functionally different. Such
RICHARDS ET AL. 585
localized changes in the temporoparietal region are less neurovascular bundle, should such distinctions exist.
likely to result from “packing issues,” because large Further, the presence of an enlarged “vein” in association
changes in cranial shape that result in packing issues with, or as a portion of, the middle meningeal neurovas-
would tend to distribute changes in brain anatomy across cular bundle, has been suggested to be a primitive trait
a wider cranial region (Yawitz et al., 2020). Further, given (Saban, 1982), an apomorphy (Arsuaga et al., 1997), or an
that white matter comprises most of the tissue deep to autapomorphy (Bruner, Averini, & Manzi, 2003a; Bruner,
the cortex in the caudal temporoparietal region, it is Manzi, & Arsuaga, 2003b) in Neanderthals (Gracia, 1991;
unlikely that it would show such localized increases in Grimaud-Hervé, 1997; Saban, 1995). We have shown that
the absence of cortical expansion. Localized expansions this venous channel is absent in Guercy 1 and most Early
of the subarachnoid space (≠interstitial space of Alatorre Neanderthals, but it is considered to be present at high
Warren et al., 2019) are also unlikely to account for the frequencies in Preneanderthals (Poza-Rey, 2015) and Late
differences, because they are not known to form in these Neanderthals (Grimaud-Hervé, 1997). Recent work on
lateral temporoparietal regions. Therefore, morphological modern human juveniles (Cronin et al., 2022) found a
changes occurring in the brains of Preneanderthals, Early low frequency of wide (≈2–3 mm) but shallow vascular
Neanderthals, and Late Neanderthals, as revealed by channels on the frontal and parietal bones that connect
analysis of endocasts, supports a mosaic model of brain the superior sagittal sinus with the other dural sinuses or
evolution that emphasizes the selective expansion of the middle meningeal system. These channels differ from
independent structural and functional modules. Such a the deep impressions related to the meningeal neurovas-
model of brain evolution, wherein brain structures with cular bundle (Cronin et al., 2022), and the veins are seen
major anatomical and functional links evolve together to be contained within the dura mater on dissection.
independently of evolutionary changes in other struc- These may represent bridging veins. Further work is nec-
tures, has been proposed by Barton and Harvey (2000). A essary to establish the relationship of these impressions
mosaic model of evolution in Middle-to-Late Pleistocene to the great anterior vein and middle meningeal venous
European/Middle Eastern hominins is further supported drainage and whether they are useful in taxonomy or
by morphological analyses of the Sima de los Huesos phylogenetic reconstructions.
paleodeme (Arsuaga et al., 1997) and the Apidima Recent reviews of the correlation between morpho-
(de Lumley et al., 2020) and Biache-Saint-Vaast remains logical change in hominin endocrania and changes in
(Martín-Francés et al., 2022). brain function are available for the frontal (Parks &
Middle meningeal neurovascular grooves and dural Smaers, 2018), parietal (Bruner, 2010, 2014; Bruner
sinus patterns have been extensively assessed in modern et al., 2022; Bruner, Amano, et al., 2018a; Bruner, Esteve-
humans and fossil hominins (middle meningeal neuro- Altava, & Rasskin-Gutman, 2018b; Bruner, Ogihara, &
vascular bundles: Giuffrida-Ruggeri, 1912; Chandler & Tanabe, 2018c), temporal (Bryant & Preuss, 2018), and
Derezinski, 1935; Rothman, 1937; Saban, 1979, 1980, occipital lobes (Todorov & de Sousa, 2018) and the cere-
1982, 1986; Grimaud-Hervé & Saban, 1996; Grimaud- bellum (Tanabe et al., 2018; Zhang & Wu, 2021).
Hervé, 1997, 2004; Ruïz et al., 2004; Tubbs et al., 2007; Although our comparative description of Guercy 1 can
Bruner & Sherkat, 2008; Bruner et al., 2009, 2011; Peña- add to these discussions, we are not contributing to them
Melian et al., 2011; Poza-Rey, 2015; Píšova et al., 2017; de at this time for two reasons. Firstly, we concur with Ala-
Lazaro et al., 2018; Cronin et al., 2022; dural sinus pat- torre Warren et al. (2019) that inferences about brain
terns: Browder et al., 1973; Grimaud-Hervé & structure from endocasts should not be carried out based
Saban, 1996; Grimaud-Hervé, 1997, 2004; Braga & on endocranial shape or neurocranial structures without
Boesch, 1997; Kopuz et al., 2010; Okudera et al., 1994; the prior identification and description of gyri and sulci,
Píšova et al., 2017). Description of the Preneanderthal which have not been fully characterized in Early Nean-
paleodeme (Poza-Rey, 2015) and a sample of recent derthals. Secondly, because the Early Neanderthal sam-
human juveniles (5.0–7.9 y: N = 69: Cronin et al., 2022) ple is constrained, both in size and neural regions
confirms Piveteau's (1970) observation of the highly vari- preserved, discussion of potential changes in neural func-
able nature of the imprint for this neurovascular bundle tion are more appropriately addressed following comple-
in these two groups. tion of our description of the more complete Guercy
The neurovascular branching pattern observed in 2 endocast.
Guercy 1 is simple and broadly like those described for
some Preneanderthals, Early Neanderthals, and Late
Neanderthals (Bruner et al., 2006; Bruner & Manzi, 2008; 5 | CONCLUSIONS
Grimaud-Hervé, 1997; Holloway et al., 2004;
Saban, 1995). Further work is needed to differentiate the Our current picture of brain evolution in Neanderthals
groups more clearly based on features of this and their precursors is hampered by incomplete
586 RICHARDS ET AL.
morphological descriptions and the inclusion of too few number: 03-Activity-059; (RSJ) Faculty Development
specimens in the published record to clarify the range of Fund of Saint Mary's College of California.
variation in Early Neanderthals. Our ongoing assessment
of the endocranial anatomy of Guercy 1 and 2 will help CONFLICT OF INTEREST
to rectify a portion of this problem. As discussed by The authors declare no conflicts of interest.
Mounier et al. (2016), combining descriptions of the
endocranial and ectocranial anatomy will lead to new DA TA AVAI LA BI LI TY S T ATE ME NT
insights into paleodemes and phylogeny. The delineation All data collected on the Moula-Guercy endocranial
of paleodemes in the European Middle-to-Late Pleisto- reconstruction and from the literature are provided
cene has been a topic of discussion for over 70 years within the main text and tables and Supplemental Data.
(Bräuer et al., 2020; Condemi, 1998, 2001, 2005; Condemi
et al., 2010; Hawks & Wolpoff, 2001; Howell, 1952, 1996, ORCID
1999; Hublin, 2002; Martín-Francés et al., 2022;
Gary D. Richards https://orcid.org/0000-0002-5675-
Roebroeks et al., 2011; Vandermeersch, 1987; 080X
Vandermeersch & Garralda, 2011). The important role of
the MIS 5e Neanderthals from Baume Moula-Guercy in
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The Anatomical Record - 2022 - Richards - Endocranial Anatomy of The Guercy 1 Early Neanderthal From Baume Moula Guercy

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Received: 1 August 2022 Revised: 29 October 2022 Accepted: 31 October 2022

Endocranial anatomy of the Guercy 1 early Neanderthal

Gary D. Richards 1 | Rebecca S. Jabbour 2 | Gaspard Guipert 3 | Alban Defleur 4

564 wileyonlinelibrary.com/journal/ar Anat Rec. 2023;306:564–593.

1 | INTRODUCTION classic descriptions of recent human and Neanderthal

Poza-Rey, 2015; Poza-Rey et al., 2019). Alternatively, in

3.6 | Endocranial neurovascular grooves

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