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The Neocortex of Cetartiodactyls. II. Neuronal Morphology of the Visual and Motor Cortices in the Giraffe (Giraffa Camelopardalis)

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The Neocortex of Cetartiodactyls. II. Neuronal Morphology of the Visual and Motor Cortices in the Giraffe (Giraffa Camelopardalis) Brain Struct Funct (2015) 220:2851–2872 DOI 10.1007/s00429-014-0830-9 ORIGINAL ARTICLE The neocortex of cetartiodactyls. II. Neuronal morphology of the visual and motor cortices in the giraffe (Giraffa camelopardalis) Bob Jacobs • Tessa Harland • Deborah Kennedy • Matthew Schall • Bridget Wicinski • Camilla Butti • Patrick R. Hof • Chet C. Sherwood • Paul R. Manger Received: 11 May 2014 / Accepted: 21 June 2014 / Published online: 22 July 2014 Ó Springer-Verlag Berlin Heidelberg 2014 Abstract The present quantitative study extends our of aspiny neurons in giraffes appeared to be similar to investigation of cetartiodactyls by exploring the neuronal that of other eutherian mammals. For cross-species morphology in the giraffe (Giraffa camelopardalis) neo- comparison of neuron morphology, giraffe pyramidal cortex. Here, we investigate giraffe primary visual and neurons were compared to those quantified with the same motor cortices from perfusion-fixed brains of three su- methodology in African elephants and some cetaceans badults stained with a modified rapid Golgi technique. (e.g., bottlenose dolphin, minke whale, humpback whale). Neurons (n = 244) were quantified on a computer-assis- Across species, the giraffe (and cetaceans) exhibited less ted microscopy system. Qualitatively, the giraffe neo- widely bifurcating apical dendrites compared to ele- cortex contained an array of complex spiny neurons that phants. Quantitative dendritic measures revealed that the included both ‘‘typical’’ pyramidal neuron morphology elephant and humpback whale had more extensive den- and ‘‘atypical’’ spiny neurons in terms of morphology drites than giraffes, whereas the minke whale and bot- and/or orientation. In general, the neocortex exhibited a tlenose dolphin had less extensive dendritic arbors. Spine vertical columnar organization of apical dendrites. measures were highest in the giraffe, perhaps due to the Although there was no significant quantitative difference high quality, perfusion fixation. The neuronal morphol- in dendritic complexity for pyramidal neurons between ogy in giraffe neocortex is thus generally consistent with primary visual (n = 78) and motor cortices (n = 65), what is known about other cetartiodactyls. there was a significant difference in dendritic spine density (motor cortex [ visual cortex). The morphology Keywords Dendrite Á Morphometry Á Dendritic spine Á Golgi method Á Brain evolution B. Jacobs (&) Á T. Harland Á D. Kennedy Á M. Schall Laboratory of Quantitative Neuromorphology, Psychology, Colorado College, 14 E. Cache La Poudre, Colorado Springs, Introduction CO 80903, USA e-mail: [email protected] In our companion paper on cetartiodactyls (Butti et al. 2014b), we documented the neuronal morphology of B. Wicinski Á C. Butti Á P. R. Hof Fishberg Department of Neuroscience and Friedman Brain three cetacean species (bottlenose dolphin, minke whale, Institute, Mount Sinai School of Medicine, One Gustave L. Levy and humpback whale). Here, we explore the neuronal Place, New York, NY 10029, USA morphology of the giraffe (Giraffa camelopardalis) for the first time. Although the long necked-giraffe’s status C. C. Sherwood Department of Anthropology, The George Washington as the tallest extant land mammal has resulted in exten- University, 2110 G Street, NW, Washington, DC 20052, USA sive investigation of its vertebral column (Solounias 1999; Badlangana et al. 2009) and cardiovascular system P. R. Manger (Nilsson et al. 1988; Badeer 1997), few studies have School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown, examined the giraffe brain beyond gross anatomy (Friant Johannesburg 2193, South Africa 1968). Recent investigations have begun to explore the 123 2852 Brain Struct Funct (2015) 220:2851–2872 implications of an elongated neck in the anatomy of (Hof et al. 1999; Sherwood et al. 2009). Given the brainstem nuclei (Badlangana et al. 2007a; Bux et al. close relationship between certain large artiodactyls 2010) and the corticospinal system (Badlangana et al. (e.g., Hippopotomidae) and cetaceans (Shimamura et al. 2007b); nevertheless, apart from some initial descriptions 1997;UrsingandArnason1998; Nikaido et al. 1999; of neurons in selected ungulates (Barasa 1960), the Price et al. 2005), we expect comparable neuromor- morphology of cortical neurons in the giraffe remains phological features across giraffes, the pygmy hippo- unknown. As part of an ongoing project documenting potamus, and cetaceans. Such a comparative neocortical neuromorphology in previously unexplored perspective provides a focal point of the current large brained mammals (Jacobs et al. 2011), the current investigation. study may further our understanding of which aspects of The giraffe, with a brain mass of between 400 and neuronal morphology are general to all vertebrates, and 700 g (Crile and Quiring 1940; Mitchell et al. 2008), has which are specific to particular species. To that end, the a relatively long gestation period and a relatively com- present investigation documents the neuronal morphology plex sociobehavioral environment (Pe´rez-Barberı´a and of the primary motor and visual cortices of the giraffe. Gordon 2005; Shultz and Dunbar 2006). They reside Within the superorder Laurasiatheria, giraffes belong within a fission–fusion, mostly matrilineal social structure to the clade Cetartiodactyla (order Artiodactyla; sub- characterized by considerable flexibility in herd size (Van order Ruminantia). Giraffidae emerged from Pecora in der Jeugd and Prins 2000; Bashaw et al. 2007; Bercov- the Oligocene period, with Giraffini diverging from itch and Berry 2013; Carter et al. 2012). Several types of their closest living relative, Okapini, approximately 19 social interaction have been documented: urine assess- million years ago (Hassanin and Douzery 2003). Extant ment to determine female reproductive status, mate laurasiatherian species (e.g., giraffe, cat, dog, horse, guarding of receptive females (Bercovitch et al. 2006), sheep, cow, seal, hippopotamus, dolphin, whale) exhibit and neck rubbing for social cohesion and bonding (Coe considerable diversity in terms of physiology, behavior, 1967; Tarou et al. 2000). Auditory and particularly visual brain mass, and encephalization quotient (Radinsky senses seem well developed (Innis 1958). The giraffe has 1981;Ferna´ndez and Vrba 2005; Boddy et al. 2012), a visual acuity of 25–27 cycles per degree, which is and thus may provide insight into the complexities and approximately half that of humans, but substantially evolutionary plasticity of mammalian neocortical evo- higher than that seen in most other Cetartiodactyls lution. In particular, comparison of evolutionary pat- (Coimbra et al. 2013). The extent to which giraffes terns and modern phylogenomic techniques underscore communicate vocally remains unclear, although it has a close relationship between cetaceans and artiodactyls, been suggested that they are among several species (e.g., which have recently been grouped in the clade Cetar- okapi, rhinoceros, elephants, whales) that may use in- tiodactyla (Nikaido et al. 1999;Murphyetal.2004; frasound (Bashaw 1993). These behaviors, coupled with a Price et al. 2005). It should be noted that the Artio- relatively large brain size, suggest considerable cognitive dactyla suborder Ruminantia appears to be most closely ability in giraffes. related to hippopotami and cetaceans, and composes a The relationship between cognitive abilities and cor- clade referred to as Cetruminantia (Graur and Higgins tical neuronal morphometry remains elusive in giraffes 1994; Shimamura et al. 1997). As such, it would be because their cerebral cortex remains largely unexplored reasonable to expect similarities in the organization of (DeFelipe et al. 2002), with only one recent study the brain among related species within cetartiodactyls examining giraffe cortex directly (Badlangana et al. (Hof and Sherwood 2005, 2007; Sherwood et al. 2009). 2007b). Therefore, in addition to qualitative classification For example, in the pygmy hippopotamus (Hexaproto- of neuronal types, the present study quantitatively don liberiensis) and cetaceans (bottlenose dolphin, investigated regional variation, with a focus on the Tursiops truncatus; minke whale, Balaenoptera acut- numerically dominant pyramidal neurons, in primary orostrata; humpback whale, Megaptera novaeangliae), motor and visual cortices. Although increased dendritic a variety of complex neocortical neurons have recently complexity has been associated with enhanced processing been documented, with spiny neurons existing along a demands in higher order primate cortices (Elston 2003, continuum from those that appeared more pyramid-like 2007; Jacobs and Scheibel 2002), there appears to be no to those that differ from the ‘‘typical’’ (i.e., primate/ a priori reason to expect differences in cortical pro- rodent-like) pyramidal neuron in terms of morphology cessing across primary cortical areas (Jacobs et al. 2001; and/or orientation (Butti et al. 2014a, b). In contrast, Clemo and Meredith 2012). As such, we expect pyra- aspiny cortical neurons appear relatively uniform and midal neuron dendritic extent to be similar between morphologically conserved across eutherian mammals giraffe primary motor and visual cortices. 123 Brain Struct Funct (2015) 220:2851–2872 2853 Materials and methods stained via a modified rapid Golgi technique (Scheibel and Scheibel 1978b), and sectioned serially at 120 lm with a Specimens vibratome (Leica VT1000S,
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