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Neocortical Neuronal Morphology in the Newborn Giraffe (Giraffa Camelopardalis Tippelskirchi) and African Elephant (Loxodonta Africana)

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Neocortical Neuronal Morphology in the Newborn Giraffe (Giraffa Camelopardalis Tippelskirchi) and African Elephant (Loxodonta Africana) RESEARCH ARTICLE Neocortical Neuronal Morphology in the Newborn Giraffe (Giraffa camelopardalis tippelskirchi) and African Elephant (Loxodonta africana) Bob Jacobs,1* Laura Lee,1 Matthew Schall,1 Mary Ann Raghanti,2 Albert H. Lewandowski,3 Jack J. Kottwitz,4 John F. Roberts,5 Patrick R. Hof,6 and Chet C. Sherwood7 1Laboratory of Quantitative Neuromorphology, Department of Psychology, Colorado College, Colorado Springs, Colorado 80903 2Department of Anthropology, Kent State University, Kent, Ohio 44242 3Cleveland Metroparks Zoo, Cleveland, Ohio 44109 4Department of Anatomy, Physiology, and Pharmacology, College of Veterinary Medicine, Auburn University, Auburn, Alabama 36849 5Thompson Bishop Sparks State Diagnostic Laboratory, Alabama Department of Agriculture and Industries, Auburn, Alabama 36849 6Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, New York 10029 7Department of Anthropology, The George Washington University, Washington, DC 20052 ABSTRACT of spiny projection neurons. Projection neurons were Although neocortical neuronal morphology has been observed in both species, with a much larger variety in documented in the adult giraffe (Giraffa camelopardalis the elephant (e.g., flattened pyramidal, nonpyramidal tippelskirchi) and African elephant (Loxodonta africana), multipolar, and inverted pyramidal neurons). Although no research has explored the cortical architecture in local circuit neurons (i.e., interneurons, neurogliaform, newborns of these species. To this end, the current Cajal–Retzius neurons) resembled those observed in study examined the morphology of neurons from several other eutherian mammals, these were usually spiny, cortical areas in the newborn giraffe and elephant. After which contrasts with their adult, aspiny equivalents. cortical neurons were stained with a modified Golgi Newborn projection neurons were smaller than the adult technique (N 5 153), dendritic branching and spine dis- equivalents in both species, but newborn interneurons tributions were analyzed by using computer-assisted were approximately the same size as their adult counter- morphometry. The results showed that newborn elephant parts. Cortical neuromorphology in the newborn giraffe is neurons were considerably larger in terms of all dendritic thus generally consistent with what has been observed and spine measures than newborn giraffe neurons. Quali- in other cetartiodactyls, whereas newborn and adult ele- tatively, neurons in the newborns appeared morphologi- phant morphology appears to deviate substantially from cally comparable to those in their adult counterparts. what is commonly observed in other placental mammals. Neurons in the newborn elephant differed considerably J. Comp. Neurol. 000:000–000, 2015. from those observed in other placental mammals, includ- ing the giraffe, particularly with regard to the morphology VC 2015 Wiley Periodicals, Inc. INDEXING TERMS: dendrite; morphometry; Golgi method; brain evolution; neocortex; nif-0000–10294 Recent investigations into the morphology of neocort- ical neurons in relatively large brained mammals have revealed evolutionarily conserved features across spe- Grant sponsor: The James S. McDonnell Foundation; Grant numbers: cies, but also some characteristics that are unique 22002078 (to P.R.H. and C.C.S.); 220020293 (to C.C.S). within phylogenetic groups. Within cetartiodactyls, *CORRESPONDENCE TO: Bob Jacobs, Ph.D., Laboratory of Quantitative pyramidal neurons are the dominant type in the neocor- Neuromorphology, Department of Psychology, Colorado College, 14 E. Cache La Poudre, Colorado Springs, CO 80903. tex, with an apical dendrite morphology that appears to E-mail: [email protected] exist along a continuum from those that are similar to Received April 28, 2015; Revised June 19, 2015; apical dendrites in ‘‘typical’’ (i.e., primate/rodent-like) Accepted June 22, 2015. DOI 10.1002/cne.23841 Published online Month 00, 2015 in Wiley Online Library VC 2015 Wiley Periodicals, Inc. (wileyonlinelibrary.com) The Journal of Comparative Neurology | Research in Systems Neuroscience 00:00–00 (2015) 1 B. Jacobs et al. pyramidal neurons (Bianchi et al., 2012) to those that tively, as was the case with the adult animals, we differ slightly in terms of apical branching profiles (e.g., expected the dendritic systems within the same neuro- humpback whale, minke whale, bottlenose dolphin: nal type to be more extensive in the newborn elephant Butti et al., 2015; pygmy hippopotamus: Butti et al., than in the newborn giraffe. Qualitatively, the newborn 2014; giraffe: Jacobs et al., 2015). In the African ele- samples allowed us to investigate whether the funda- phant neocortex, however, neuronal morphology is dis- mental neuromorphological differences we observed tinct from all other placental mammals examined to between the adult elephant and giraffe also obtained in date (Jacobs et al., 2011), including other afrotherians newborn animals. In general, we expected the newborn like the rock hyrax (Bianchi et al., 2011). Specifically, giraffe neocortex to exhibit a more typical columnar differences in the elephant projection neurons are man- organization, with vertically ascending apical dendrites, ifested not only in apical dendrite morphology, which is than the newborn elephant neocortex, which would be characterized by widely bifurcating rather than singu- characterized by widely bifurcating apical dendrites and larly ascending apical dendrites (Mountcastle, 1997; a greater variety of neuronal morphologies that are Innocenti and Vercelli, 2010), but also by the preva- unlike those characteristic of anthropoid primate and lence of several horizontally oriented spiny neurons murid rodent models. In contrast, little variation was such as flattened pyramidal and nonpyramidal multipo- expected for local circuit neurons (e.g., interneurons, lar neurons (Jacobs et al., 2011). The neuronal morphol- neurogliaform, and Cajal–Retzius neurons) between the ogy observed in these species to date, however, has two species, as these neurons have been shown to be been limited to the adult neocortex. The present study relatively uniform and morphologically conserved across addresses this deficit by exploring the neuronal mor- eutherian mammals (Hof et al., 1999; Sherwood et al., phology in several neocortical regions of the newborn 2009). giraffe (Giraffa camelopardalis tippelskirchi) and African elephant (Loxodonta africana). The availability of well- MATERIALS AND METHODS preserved newborn brain tissue in both the elephant and giraffe presented a rare opportunity not only to ver- Specimens Cortical samples were obtained from a newborn ify our neuromorphological findings in the adults (Jacobs et al., 2011, 2015), but also to document neu- giraffe (Giraffa camelopardalis tippelskirchi) and a new- ronal types early in development. born African elephant (Loxodonta africana). The brain of Although neocortical neuronal development has been a 1-day old female giraffe with failure to thrive (378 g; extensively investigated in primates (Lund et al., 1977; autolysis time [AT] 5 6 hours) was provided by the Marin-Padilla, 1992; Travis et al., 2005; Bianchi et al., Cleveland Metroparks Zoo. The brain of a stillborn male 2013; Elston and Fujita, 2014), rodents (Parnavelas elephant (1,745 g; AT < 12 hours) was provided by the et al., 1978; Miller, 1981) and, to a lesser extent, Alabama Veterinary Diagnostic Laboratories, Auburn. felines (Marin-Padilla, 1971, 1972), there is little neuro- Both brains were immersion-fixed in 10% formalin developmental information for other, relatively large (giraffe: 30 days; elephant: 10 months). Cortical areas brained species (Manger, 2008). Giraffes and especially of interest were removed and stored in 0.1 M elephants have prolonged developmental periods, with phosphate-buffered saline (PBS) with 0.1% sodium azide substantial increases in brain size from the neonate to for 3 months prior to Golgi staining. The present study the adult. In giraffes, biological measures indicate that was approved by the Colorado College Institutional sexual maturity is reached at 4–5 years of age (Hall- Review Board (#011311-1). Martin et al., 1978). In elephants, sexual maturity is reached at 15 years of age, although successful Tissue selection reproduction for males can take 10–20 more years In the giraffe, tissue blocks (3–5 mm thick) were (Millar and Zammuto, 1983; Moss and Lee, 2011). Pro- removed from the primary motor and visual cortices of longed postnatal neurodevelopmental periods are also the right hemisphere (Fig. 1). Motor cortex tissue was common in many mammals (Sacher and Staffeldt, located anteriorly on the dorsomedial aspect of the cer- 1974). Thus, given the relatively immature size of the ebrum (Badlangana et al., 2007), and was removed newborn brains examined in the present study, we about 1–2 cm lateral to the longitudinal fissure; visual expected the neurons in our sample to be significantly cortex tissue was located posteriorly on the dorsome- smaller than their adult counterparts. dial aspect of the cerebrum and was removed about Based on our previous examination of neurons in 2–3 cm lateral to the longitudinal fissure (Fig. 1). In the adult giraffe and elephant neocortex (Jacobs et al., elephant, tissue blocks (3–5 mm thick) were removed 2011, 2015), two other predictions follow. Quantita- from the frontal, motor, and occipital (i.e., putative 2 The Journal of Comparative Neurology | Research in Systems Neuroscience
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