Hominoid visual brain structure volumes and the position of the lunate sulcus

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Abstract

It has been argued that changes in the relative sizes of visual system structures predated an increase in brain size and provide evidence of brain reorganization in hominins. However, data about the volume and anatomical limits of visual brain structures in the extant taxa phylogenetically closest to humans–the apes–remain scarce, thus complicating tests of hypotheses about evolutionary changes. Here, we analyze new volumetric data for the primary visual cortex and the lateral geniculate nucleus to determine whether or not the human brain departs from allometrically-expected patterns of brain organization. Primary visual cortex volumes were compared to lunate sulcus position in apes to investigate whether or not inferences about brain reorganization made from fossil hominin endocasts are reliable in this context. In contrast to previous studies, in which all species were relatively poorly sampled, the current study attempted to evaluate the degree of intraspecific variability by including numerous hominoid individuals (particularly Pan troglodytes and Homo sapiens). In addition, we present and compare volumetric data from three new hominoid species–Pan paniscus, Pongo pygmaeus, and Symphalangus syndactylus. These new data demonstrate that hominoid visual brain structure volumes vary more than previously appreciated. In addition, humans have relatively reduced primary visual cortex and lateral geniculate nucleus volumes as compared to allometric predictions from other hominoids. These results suggest that inferences about the position of the lunate sulcus on fossil endocasts may provide information about brain organization.

Introduction

The primary visual cortex (V1) receives visual information directly from the lateral geniculate nucleus (LGN) in the thalamus, which in turn receives information from the retinal ganglion cells via the optic nerve. In humans, V1 appears to be smaller than would be predicted for a primate of our brain size (Filimonoff, 1933, Frahm et al., 1984, Holloway, 1997), and LGN is smaller than predicted for a primate of our brain size (Holloway, 1997). It has been suggested that this pattern reflects an increase in brain tissue allocated to higher order functions, and does not reflect a reduction in visual information processing (Holloway, 1997), because comparable visual acuity has been demonstrated for humans and macaques (Macaca; De Valois et al., 1974). In fact, the absolute volume of V1 in humans exceeds that of all other primates (Frahm et al., 1984, Bush and Allman, 2004), although it does not keep pace with the three-fold expansion of human neocortex over that of great apes.

In fossil hominins, evidence for changes in V1 volume have been inferred from the position of the lunate sulcus (also called the Affenspalte or simian sulcus), a gross anatomical landmark approximately coincident with the lateral-anterior limit of V1 in apes and some monkey species (Fig. 1; von Bonin and Bailey, 1947, Holloway et al., 2003a). Dart (1925) observed a posteriorly-positioned lunate sulcus in the Taung (Australopithecus africanus) endocast, and suggested that this indicates enlargement of posterior parietal association cortex at the expense of V1 volume. Posterior parietal areas have specialized multisensory and motor functions in behaviors which include gesturing (Creem-Regehr, 2009), action planning (Coulthard et al., 2008), tool use (Peeters et al., 2009), and stone tool making (Stout et al., 2008). In contrast, V1 is entirely visual in function and relatively unspecialized. Although Dart's interpretation of the lunate sulcus in Taung has been questioned (Falk, 1980), another endocast, Stw 505, has been proposed to provide better evidence for a posteriorly-positioned lunate sulcus in Australopithecus africanus (Holloway et al., 2004b). Holloway, 1966, Holloway, 1975, Holloway, 1985) has discussed in detail the notion that brain reorganization might have enabled small-brained early hominins to engage in more complex behaviors.

There are two potential problems with relying on the lunate sulcus as an indication of brain organization. First, although sulci are often used as landmarks for determining the size of cortical regions in hominoids, they do not reliably delimit cytoarchitectonic areas (Amunts et al., 2007b). In fact, correspondence between histologically-defined V1 volume and the extent of the lunate sulcus has not been demonstrated in apes. However, current evidence shows that the position of the lunate sulcus indicates the extent of the lateral part of V1 in chimpanzees (Pan trogolodytes; including two specimens with lunate sulci in unusually posterior positions; Holloway et al., 2003b). In fact, Smith (1903) and Black (1915) considered a relationship to striate cortex to be a requirement for lunate sulcus identification in humans, based on the observation that the lunate sulcus delimits V1 in the species in which it occurs (Brodmann, 1906, Ingalls, 1914). However, it is possible that the lunate sulcus is only an indication of the lateral-anterior limit of V1, and does not correlate with total V1 volume in closely related hominoid species. In humans Ono et al. (1990) report that a lunate sulcus is present in 60% of right and 64% of left hemispheres (n = 25), although Allen et al. (2006) argue that “true” lunate sulci are much rarer, only occurring in 1.4% of human hemispheres (n = 220). In humans, the sulcus best associated with the extent of V1 is the calcarine sulcus, which is located on the medial surface of the hemispheres. However, Gilissen et al. (1995) suggest that V1 volume cannot be inferred from calcarine sulcus length in human brains (n = 23) because the depth of the sulcus varies considerably.

Second, it is possible that reduced relative V1 volume can be attributed to increased brain size, unrelated to functionally-relevant changes in brain organization. Across primates, V1 volume scales with negative allometry to brain size (Frahm et al., 1984, Bush and Allman, 2004), so it is possible that reduction in relative V1 volume in humans is simply an extension of this allometric relationship. It has also been suggested that the position of the lunate sulcus is directly related to brain size–in bigger brained species, the extent of V1 is shifted from a more-lateral to a more-medial position–and therefore, the lunate sulcus cannot occur in a posterior position on a small-brained hominoid (Jerison, 1975).

Several hypotheses have been proposed to explain observations about the negative allometric scaling of V1 volume to overall brain volume. Kaas (2000) hypothesized that, as cortical areas increase in surface area, it becomes more difficult to maintain connections among them, and as a result, the number of cortical areas increases. This is supported by the finding that across mammals the number of neocortical areas (and the number of areas to which each is connected) scale to the 1/3 power of the volume of the cerebral cortex (Changizi and Shimojo, 2005). Thus, as a general rule, larger brains tend to have a greater number of visual areas. The role of the primary cortical area in information processing is expected to decrease as its specific functions are delegated to an increasing number of higher order cortical areas. It follows that the relatively large macaque V1 would be more generalized in function than the relatively small human V1. Although such physiological differences have not yet been demonstrated, histological differences between human and macaque V1 have been established (Preuss et al., 1999, Preuss and Coleman, 2002).

We measured the volume of V1 and other brain structures in hominoids and a crab-eating macaque (Macaca fascicularis) to test the hypothesis that the human V1 volume can be predicted from allometrically-expected patterns of brain organization. Additionally, nonhuman hominoid brains were three-dimensionally reconstructed such that V1 volumes could be compared to the position of the lunate sulcus. In particular, this study sets out to examine whether or not previous findings that humans have significantly reduced V1 and LGN volumes can be confirmed for a larger comparative sample of hominoid brains, and whether or not the lunate sulcus serves as a reliable predictor of V1 volume in nonhuman hominoid species. Using these new comparative visual structure volume data from hominoids, we further examine the suggestion that humans differ from nonhuman hominoid species in the relative size of specific brain regions, but that these differences are small compared to differences in visual system structures (Holloway, 1997, Holloway, 2002).

Section snippets

Specimens and tissue preparation

Measurements were taken on histological sections from a total of 29 brains representing seven hominoid species, plus one cercopithecoid species. We used sections from the left hemispheres of adult specimens, including a range of ages and both sexes (Table 1). To accumulate a large and diverse sample, specimens in the study come from several different collections: the Zilles and Stephan comparative neuroanatomy collections at C&O Vogt Institute of Brain Research in Düsseldorf, Germany, the

Absolute visual structure volumes

Among hominoids, absolute left V1 volume is greatest in humans, and lowest in the hylobatids, which are phylogenetically most distant from humans. The mean and inter-individual variability in the human sample reported here (n = 10; mean = 7.62 cm3; CV = 0.23) is similar to that reported in a previous study (n = 9; mean = 7.91 cm3; CV = 0.19; Gilissen and Zilles, 1995). The range of variation in human V1 volume is similar to that for chimpanzee V1 volume (Pan troglodytes n = 7; mean = 4.13 cm3; CV = 0.20) and

Human predictions

The main purpose of this study was to determine whether brain reorganization in H. sapiens is manifest in an unusually small V1 volume for its brain size. Because the LGN is the primary source of inputs to V1, the relationship of LGN size to brain size, and V1 size to LGN size, were also considered to provide a wider scope within which to interpret the findings. Our results demonstrate that human V1 and LGN volumes are smaller than expected for a primate of similar brain volume. Specifically,

Conclusions

This study provides evidence for gross-level brain reorganization within the hominoids and catarrhines, with respect to the relative size of V1 and LGN. V1 volumes are quite variable within and among hominoid species, supporting earlier findings that, within the hominin lineage, V1 volume is smaller than expected for a primate of similar brain size. Furthermore, V1 volume is predictable from lunate sulcus position in apes. Therefore, evidence of posteriorly-positioned lunate sulci in early

Acknowledgements

We are grateful to Drs. Bernard Wood, Ralph Holloway, Peter Lucas, and Brian Richmond for comments on earlier versions of the manuscript. Dr. Katerina Semendeferi was instrumental in establishing the Zilles ape brain collection used in this study. Dr. Joseph Erwin facilitated access to great ape brain specimens. The Yerkes Primate Center also provided brains. This work was supported by the National Science Foundation (BCS-9987590, BCS-0453005, BCS-0515484, BCS-0549117, BCS-0827531, DGE-0801634

References (87)

  • C.E. MacLeod et al.

    Expansion of the neocerebellum in Hominoidea

    J. Hum. Evol.

    (2003)
  • B. Merker

    Silver staining of cell bodies by means of physical development

    J. Neurosci. Methods

    (1983)
  • P.E. Roland et al.

    Brain atlases–a new research tool

    Trends Neurosci.

    (1994)
  • C.F. Ross et al.

    Curvilinear, geometric and phylogenetic modeling of basicranial flexion: is it adaptive, is it constrained?

    J. Hum. Evol.

    (2004)
  • J.S. Allen et al.

    Looking for the lunate sulcus: a magnetic resonance imaging study in modern humans

    Anat. Rec.

    (2006)
  • J. Allman et al.

    Visual cortex in primates

    Comparative Primate Biology

    Neurosciences

    (1988)
  • K. Amunts et al.

    Gender-specific left-right asymmetries in human visual cortex

    J. Neurosci.

    (2007)
  • D. Black

    A note on the sulcus lunatus in man

    J. Comp. Neurol.

    (1915)
  • K. Brodmann

    Beiträge zur histologischen Lokalisation der Grosshirnrinde. 5. Mitteilung: über die allgemeinen Bauplan des Cortex palii bei den Mammalieren und zwei homologe Rindenfelder im besonderem. Zugleich ein Beitrag zur Furchenlehre

    J. Psychol. Neurol

    (1906)
  • E. Bruner

    Cranial shape and size variation in human evolution: structural and functional perspectives

    Childs Nerv. Syst.

    (2007)
  • E. Bruner et al.

    Encephalization and allometric trajectories in the genus Homo: evidence from the Neandertal and modern lineages

    Proc. Natl. Acad. Sci. U S A

    (2003)
  • E.C. Bush et al.

    Three-dimensional structure and evolution of primate primary visual cortex

    Anat. Rec.

    (2004)
  • M.A. Changizi et al.

    Parcellation and area-area connectivity as a function of neocortex size

    Brain Behav. Evol.

    (2005)
  • T.H. Clutton-Brock et al.

    Comparison and adaptation

    Proc. R. Soc. Lond. B Biol. Sci.

    (1979)
  • R.A. Dart

    Australopithecus africanus: the man-ape of South Africa

    Nature

    (1925)
  • A.A. de Sousa et al.

    Comparative cytoarchitectural analyses of striate and extrastriate areas in hominoids

    Cereb. Cortex

    (2009)
  • T. Deacon

    Problems of ontogeny and phylogeny in brain-size evolution

    Int. J. Primatol.

    (1990)
  • J.F. Deegan et al.

    Spectral sensitivity of gibbons: Implications for photopigments and color vision

    Folia Primatol.

    (2001)
  • C. Dehay et al.

    Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex

    J. Comp. Neurol.

    (1996)
  • D. Falk

    A reanalysis of the South African australopithecine natural endocasts

    Am. J. Phys. Anthropol.

    (1980)
  • J. Felsenstein

    Phylogenies and the comparative method

    Am. Nat.

    (1985)
  • I.N. Filimonoff

    Über die Variabilität der Großhirnrindenstruktur. Mitteilung III. Regio occipitalis bei der höheren und niederen Affen

    J. Psychol. Neurol.

    (1933)
  • H.D. Frahm et al.

    Comparison of brain structure volumes in insectivora and primates. V. Area striata (AS)

    J. Hirnforsch.

    (1984)
  • F. Gallyas

    A principle for silver staining of tissue elements by physical development

    Acta Morphol. Acad. Sci. Hung.

    (1971)
  • T. Garland et al.

    Procedures for the analysis of comparative data using phylogenetically independent contrasts

    Syst. Biol.

    (1992)
  • T. Garland et al.

    Using the past to predict the present: Confidence intervals for regression equations in phylogenetic comparative methods

    Am. Nat.

    (2000)
  • T. Garland et al.

    Polytomies and phylogenetically independent contrasts: examination of the bounded degrees of freedom approach

    Syst. Biol.

    (1999)
  • S. Geyer et al.

    Two different areas within the primary motor cortex of man

    Nature

    (1996)
  • E. Gilissen et al.

    Is the length of the calcarine sulcus associated with the size of the human visual cortex? A morphometric study with magnetic resonance tomography

    J. Hirnforsch.

    (1995)
  • E. Gilissen et al.

    The relative volume of the primary visual-cortex and its intersubject variability among humans - a new morphometric study

    C.R. Acad. Sci. IIA

    (1995)
  • S.J. Gould

    Allometry and size in ontogeny and phylogeny

    Biol. Rev. Camb. Philos. Soc.

    (1966)
  • R.L. Holloway

    Cranial capacity, neural reorganization, and hominid cvolution - search for more suitable parameters

    Am. Anth.

    (1966)
  • R.L. Holloway

    Early hominid endocasts: volumes, morphology and significance

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