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Comparative Neocortical Neuromorphology in Felids: African Lion, African Leopard, and Cheetah

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Comparative Neocortical Neuromorphology in Felids: African Lion, African Leopard, and Cheetah Received: 8 August 2019 Revised: 18 November 2019 Accepted: 18 November 2019 DOI: 10.1002/cne.24823 RESEARCH ARTICLE Comparative neocortical neuromorphology in felids: African lion, African leopard, and cheetah Vivian T. Nguyen1 | Riri Uchida1 | Allysa Warling1 | Lucy J. Sloan1 | Mark S. Saviano1 | Bridget Wicinski2 | Therese Hård3 | Mads F. Bertelsen4 | Cheryl D. Stimpson5 | Kathleen Bitterman6 | Matthew Schall1 | Patrick R. Hof2 | Chet C. Sherwood5 | Paul R. Manger6 | Muhammad A. Spocter6,7 | Bob Jacobs1 1Laboratory of Quantitative Neuromorphology, Neuroscience Program, Abstract Department of Psychology, Colorado College, The present study examines cortical neuronal morphology in the African lion Colorado Springs, Colorado (Panthera leo leo), African leopard (Panthera pardus pardus), and cheetah (Acinonyx 2Nash Family Department of Neuroscience and Friedman Brain Institute, Icahn School of jubatus jubatus). Tissue samples were removed from prefrontal, primary motor, and Medicine at Mount Sinai, New York, New York primary visual cortices and investigated with a Golgi stain and computer-assisted 3Borås Zoo, Borås, Sweden morphometry to provide somatodendritic measures of 652 neurons. Although neu- 4Center for Zoo and Wild Animal Health, Copenhagen Zoo, Frederiksberg, Denmark rons in the African lion were insufficiently impregnated for accurate quantitative den- 5Department of Anthropology and Center for dritic measurements, descriptions of neuronal morphologies were still possible. the Advanced Study of Human Paleobiology, Qualitatively, the range of spiny and aspiny neurons across the three species was The George Washington University, Washington, District of Columbia similar to those observed in other felids, with typical pyramidal neurons being the 6 School of Anatomical Sciences, Faculty of most prominent neuronal type. Quantitatively, somatodendritic measures of typical Health Sciences, University of the Witwatersrand, Johannesburg, South Africa pyramidal neurons in the cheetah were generally larger than in the African leopard, 7Department of Anatomy, Des Moines despite similar brain sizes. A MARsplines analysis of dendritic measures correctly dif- University, Des Moines, Iowa ferentiated 87.4% of complete typical pyramidal neurons between the African leop- Correspondence ard and cheetah. In addition, unbiased stereology was used to compare the soma size Bob Jacobs, Laboratory of Quantitative of typical pyramidal neurons (n = 2,238) across all three cortical regions and Neuromorphology, Neuroscience Program, Department of Psychology, Colorado College, gigantopyramidal neurons (n = 1,189) in primary motor and primary visual cortices. 14 E. Cache La Poudre, Colorado Springs, CO Both morphological and stereological analyses indicated that primary motor 80903. Email: [email protected] gigantopyramidal neurons were exceptionally large across all three felids compared to other carnivores, possibly due to specializations related to the felid musculoskele- Funding information IOER R&G Grant Des Moines University (M.A. tal systems. The large size of these neurons in the cheetah which, unlike lions and S); South African National Research leopards, does not belong to the Panthera genus, suggests that exceptionally enlarged Foundation (P.R.M.); The James S. McDonnell Foundation, Grant/Award Number: 22002078 primary motor gigantopyramidal neurons evolved independently in these felid (to P.R.H. and C.C.S.) and 220020293 (C.C.S.) species. Peer Review The peer review history for this article is KEYWORDS available at https://publons.com/publon/10. cerebral cortex, dendrites, gigantopyramidal neuron, Golgi stain, pyramidal neuron, RRID: 1002/cne.24823. SCR_001775, RRID:SCR_001905, RRID:SCR_002526 J Comp Neurol. 2019;1–31. wileyonlinelibrary.com/journal/cne © 2019 Wiley Periodicals, Inc. 1 2 NGUYEN ET AL. 1 | INTRODUCTION This atypical felid is thus an important comparison point for neuromorphological analysis. In the last decade, the neocortical neuronal morphology of relatively rare Qualitatively, previous neuromorphological findings have docu- large-brained mammals has been explored within a comparative frame- mented considerable similarity across both domestic (Hübener, work (African elephant: Jacobs et al., 2011; cetaceans: Butti et al., 2015; Schwarz, & Bolz, 1990; Kaiserman-Abramof & Peters, 1972; Matsubara, giraffe: Jacobs, Harland, et al., 2015). The two most recent studies in this Chase, & Thejomayen, 1996; Winer, 1984) and nondomestic (Jacobs series examined nondomestic feliforms. Johnson et al. (2016) explored a et al., 2018; Johnson et al., 2016) felids. Therefore, we expect variety of cortical neuron types in the Siberian tiger and clouded leopard, neocortices in the present sample to exhibit predominantly vertically ori- noting that, consistent with Brodmann's (1909) initial observations, ented typical pyramidal neurons, along with several other neuronal types gigantopyramidal neurons in carnivore primary motor cortex (M1) were (e.g., extraverted pyramidal, gigantopyramidal, aspiny neurons). Although extremely large. Subsequently, Jacobs et al. (2018) examined both typi- quantitative differences in regional dendritic extent have been docu- cal pyramidal and gigantopyramidal neurons in M1 using two methodol- mented for pyramidal neurons in primate (Bianchi et al., 2013; Elston & ogies: a Golgi technique to provide qualitative and quantitative Rockland, 2002; Jacobs et al., 2001) and African elephant (Jacobs et al., somatodendritic measures across 19 mammalian species from 7 orders, 2011) neocortex, similar regional differences have not been observed in including several feliforms (e.g., African lion, caracal, clouded leopard, the Siberian tiger or the clouded leopard (Johnson et al., 2016). As such, and Siberian tiger), and unbiased stereology to compare soma size across there is no a priori reason to expect such differences in the current sam- 11 carnivores (including African leopard, African lion, caracal, and Sibe- ple. In addition, cross-species comparisons suggest that increased brain rian tiger) and 9 primate species. Both analyses revealed that M1 size is positively correlated with greater somatodendritic measures gigantopyramidal neurons were larger in feliforms (especially in the within mammalian lineages (Butti et al., 2015; Elston & Manger, 2014; Panthera species) than in other (sub)orders, presumably due to speciali- Jacobs, Harland, et al., 2015; Johnson et al., 2016). The average brain zations of the felid neuromusculoskeletal systems. The present study is mass of the African lion (~220 g) is twice that of both the cheetah thus a direct extension of both Johnson et al. (2016) and Jacobs et al. (~110 g) and the African leopard (~120 g; Gittleman, 1986). Therefore, (2018). Employing measurements of both dendritic morphology and we expected that the African lion neurons would be more dendritically soma size, the present study examines neocortical neuron types in the complex than those from the other two felids in the present study. prefrontal cortex, M1, and primary visual cortex (V1) of the African lion Unfortunately, because of the suboptimal quality of the Golgi stain in (Panthera leo leo), the African leopard (Panthera pardus pardus), and the the lion tissue, only a qualitative description of these dendritic systems cheetah (Acinonyx jubatus jubatus), with stereological results also com- was possible. However, these descriptive results still broaden the pared to other species of Carnivora. neuromorphological findings of Jacobs et al. (2018), which focused only These three members of the family Felidae emerged from the on pyramidal and gigantopyramidal neurons in M1 cortex. Finally, soma order Carnivora in the late Oligocene epoch ~35 million years ago size comparisons across all three species were possible with data from (Ma; Kleiman & Eisenberg, 1973). Both the African lion and African unbiased stereological analyses. leopard are members of the Panthera genus, the first of eight clades Both Golgi and stereological techniques also provided size com- within the felids to diverge ~10.8 Ma (Janczewski, Modi, Stephens, & parisons of gigantopyramidal neuron somata across the three species. O'Brien, 1995; O'Brien & Johnson, 2005). Moreover, phylogenetic Given previous findings for Panthera, M1 gigantopyramidal neurons in analyses (chemical signaling: Bininda-Emonds, Decker-Flum, & both the African lion and African leopard were expected to be excep- Gittleman, 2001; mitochondrial DNA control region: Jae-Heup, tionally large relative to other carnivore species, potentially due to Eizirik, O'Brien, & Johnson, 2001; genomic assessment: Yu & Zhang, their specialized hunting behaviors (Jacobs et al., 2018; Johnson et al., 2005) suggest that they are sister taxa, with the African lion being 2016). However, the somatodendritic characteristics of M1 one of the largest extant felids (males: ~187 kg; females: ~124 kg; gigantopyramidal neurons in the cheetah have not been documented Smuts, Robinson, & Whyte, 2009). The ~50 kg African leopard is a previously. The morphology of these neurons is of particular interest descendant of an early branch in the clade and the most prominent because the cheetah is a distant non-Panthera felid that exemplifies subspecies of the six geographically isolated groups that compose extraordinary running speed, reaching sprints of >100 km/h when the leopard lineage (Panthera pardus; Miththapala, Seidensticker, & catching prey (Sharp, 1997). To achieve this, cheetahs exhibit a modi-
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