Abstract
Here we describe the nuclear organization of the African elephant amygdaloid complex using Nissl, myelin, and a range of immunohistochemical stains. The African elephant is thought to exhibit many affect-laden and social-empathic behaviours; however, to date the amygdaloid complex, which is the generator of emotional states of the brain is yet to be fully explored in the elephants. For the most part, the amygdaloid complex of the African elephant is similar to that observed in other mammals in terms of the presence of nuclei and their topological relationships; however, we did observe several specific differences in amygdaloid organization. The elephant amygdala has undergone rotation in both the coronal and sagittal planes, seemingly associated with the expansion of the temporal lobe. Numerous scalloped cell clusters, termed glomeruli, forming the intermediate nuclei of the basal, accessory basal and central nuclear groups, were occupied by structures immunopositive to doublecortin. The nuclei typically associated with the accessory olfactory system (posterior cortical nucleus and medial nuclear complex) were absent from the elephant amygdala. The anterior cortical nucleus is very large and appears to be comprised of two subdivisions. The lateral nuclear complex is expanded and has two novel subdivisions. The amygdalohippocampal area appears relatively enlarged. The numerous shared and derived characters make the elephant amygdaloid complex very unusual and unique amongst mammals, but the derived characters appear to relate to observed elephant affect-laden behaviours.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABi:
-
Accessory basal nucleus, intermediate division
- ABmc:
-
Accessory basal nucleus, magnocellular division
- ABpc:
-
Accessory basal nucleus, parvocellular division
- ABs:
-
Accessory basal nucleus, shell
- AHiA:
-
Amygdalohippocampal area
- Bmc:
-
Basal nucleus, magnocellular division
- Bi:
-
Basal nucleus, intermediate division
- Bpc:
-
Basal nucleus, parvocellular division
- CA1:
-
Cornu ammonis region 1 of hippocampus
- CA3:
-
Cornu ammonis region 3 of hippocampus
- CeC:
-
Central amygdaloid nucleus, capsular division
- CeI:
-
Central amygdaloid nucleus, intermediate division
- CeL:
-
Central amygdaloid nucleus, lateral division
- CeM:
-
Central amygdaloid nucleus, medial division
- CoAd:
-
Anterior cortical amygdaloid nucleus, dorsal division
- CoAv:
-
Anterior cortical amygdaloid nucleus, ventral division
- DG:
-
Dentate gyrus of hippocampus
- f:
-
Fornix
- I:
-
Intercalated island of the amygdala
- ic:
-
Internal capsule
- IMG:
-
Amygdaloid intramedullary gray matter
- LAdl:
-
Lateral amygdaloid nucleus, dorsolateral part
- LAm:
-
Lateral amygdaloid nucleus, medial part
- LAvl:
-
Lateral amygdaloid nucleus, ventrolateral part
- LV:
-
Lateral ventricle
- P:
-
Putamen
- PACl:
-
Periamygdaloid cortex, lateral division
- PACm:
-
Periamygdaloid cortex, medial division
- PIR:
-
Piriform cortex
- Sub:
-
Subiculum
References
Bagley KR, Goodwin TE, Rasmussen LEL, Schulte BA (2006) Male African elephant, Loxodonta africana, can distinguish oestrus status via urinary signals. Anim Behav 71:1439–1445. https://doi.org/10.1016/j.anbehav.2006.01.003
Barger N, Stefanacci L, Semendeferi K (2007) A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. Am J Phys Anthropol 134:392–403. https://doi.org/10.1002/ajpa.20684
Barger N, Stefanacci L, Schumann CM, Sherwood CC, Annese J, Allman JM, Buckwalter JA, Hof PR, Semendeferi K (2012) Neuronal populations in the basolateral nuclei of the amygdala are differentially increased in humans compared to apes: a stereological study. J Comp Neurol 520:3035–3054. https://doi.org/10.1002/cne.23118
Bates LA, Sayialel KN, Njiraini NW, Moss CJ, Poole JH (2007) Elephants classify human ethic groups by odor and garment color. Curr Biol 17:1938–1942. https://doi.org/10.1016/j.cub.2007.09.060
Bergan JF, Ben-Shaul Y, Dulac C (2014) Sex-specific processing of social cues in the medial amygdala. eLIFE 3:e02743. https://doi.org/10.7554/eLife.02743.001
Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals—a theme with many variations. Eur J Neurosci 34:930–950. https://doi.org/10.1111/j.1460-9568.2011.07832.x
Bouley DM, Alarcon CN, Hildebrandt T, O’Connell-Rodwell CE (2007) The distribution, density and three-dimensional histomorphology of Pacinian corpuscles in the foot of the Asian elephant (Elephas maximus) and their potential role in seismic communication. J Anat 211:426–435. https://doi.org/10.1111/j.1469-7589.2007.00792.x
Doty RL, Brugger WE, Jurs PC, Orndorff MA, Snyder PJ, Lowry LD (1978) Intranasal trigeminal stimulation from odorous volatiles: pyschometric responses from anosmic and normal humans. Physiol Behav 20:175–187. https://doi.org/10.1016/0031-9384(78)90070-7
Fudge JL, Decampo DM, Becoats KT (2012) Revisiting the hippocampal-amygdala pathway in primates: association with immature-appearing neurons. Neuroscience 212:104–119. https://doi.org/10.1016/j.neuroscience.2012.03.040
Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209. https://doi.org/10.1080/01616412.1979.11739553
Gobbel L, Fischer MS, Smith TD, Wible JR, Bhatnagar KP (2004) The vomeronasal organ and associated structures of the fetal African elephant, Loxodonta africana (Proboscidea, Elephantidae). Acta Zool 85:41–52. https://doi.org/10.1111/j.0001-7272.2004.00156.x
Gould E (2007) How widespread is adult neurogenesis in mammals? Nature Rev Neurosci 8:481–487. https://doi.org/10.1038/nrn2147
Greenwood DR, Comeskey D, Hunt MB, Rasmussen EL (2005) Chemical communication: chirality in elephant pheromones. Nature 438:1097–1098. https://doi.org/10.1038/4381097a
Gross CG (1994) How inferior temporal cortex became a visual area. Cereb Cortex 4:455–469. https://doi.org/10.1093/cercor/4.5.455
Hakeem AY, Hof PR, Sherwood CC, Switzer RC, Rasmussen LE, Allman JM (2005) Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images. Anat Rec 287A:1117–1127. https://doi.org/10.1002/ar.a.20255
Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephant fit in? Neurosci Biobehav Rev 32:86–98. https://doi.org/10.1016/j.neubiorev.2007.05.012
Herculano-Houzel S, Avelino de Sousa K, Neves K, Porfirio J, Messeder D, Mattos Feijo L, Maldonado J, Manger PR (2014) The elephant brain in numbers. Front Neuroanat 8:46. https://doi.org/10.3389/fnana.2014.00046
Johnson EW, Rasmussen L (2002) Morphological characteristics of the vomeronasal organ of the newborn Asian elephant (Elephant maximus). Anat Rec 267:252–259. https://doi.org/10.1002/ar.10112
Lauer EW (1982) Telencephalon of ungulates, Chap 13. In: Crosby EC, Schnitzlein HN (eds) Comparative correlative neuroanatomy of the vertebrate telencephalon. MacMillan Publishing Co. Inc., New York, pp 501–524
LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23:155–184. https://doi.org/10.1146/annurev.neuro.23.1.155
Lee PC, Moss CJ (1999) The social context for learning and behavioural development among wild African elephants. In: Box HO, Gibson HR (eds) Mammalian social learning. Cambridge University Press, Cambridge UK, pp 102–125
Limacher-Burrell AM, Bhagwandin A, Gravett N, Maseko BC, Manger PR (2016) Nuclear organization of the rock hyrax (Procavia capensis) amygdaloid complex. Brain Struct Funct 221:3171–3191. https://doi.org/10.1007/s00429-015-1094-8
Manger PR, Pillay P, Maseko BC, Bhagwandin A, Gravett N, Moon DJ, Jillani NE, Hemingway J (2009) Acquisition of the brain of the African elephant (Loxodonta africana): perfusion-fixation and dissection. J Neurosci Meth 179:16–21. https://doi.org/10.1016/j/neumeth.2009.01.001
Maseko BC, Patzke N, Fuxe K, Manger PR (2013) Architectural organization of the African elephant diencephalon and brainstem. Brain Behav Evol 82:83–128. https://doi.org/10.1159/000352004
McComb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs are repositories of social knowledge in African elephants. Science 292:491–494. https://doi.org/10.1126/science.1057895
McComb K, Shannon G, Sayialel KN, Moss C (2014) Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. Proc Natl Acad Sci USA 111:5433–5438. https://doi.org/10.1073/pnas.1321543111
Migaud M, Batailler M, Segura S, Duittoz A, Franceschini I, Pillon D (2010) Emerging new sites for adult neurogenesis in the mammalian brain: a comparative study between the hypothalamus and the classical neurogenic zones. Eur J Neurosci 32:2042–2052. https://doi.org/10.1111/j.1460-9568.2010.07521.x
Ngwenya A, Patkze N, Ihunwo AO, Manger PR (2011) Organisation and chemical neuroanatomy of the African elephant (Loxodonta africana) olfactory bulb. Brain Struct Funct 216:403–416. https://doi.org/10.1007/s00429-01100316-y
Niimura Y, Matsui A, Touhara K (2014) Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res 24:1485–1496. https://doi.org/10.1101/gr.169532.113
O’Connell-Rodwell CE (2007) Keeping an “ear” to the ground: seismic communication in elephants. Physiology 22:287–294. https://doi.org/10.1152/physiol.00008.2007
O’Connell-Rodwell CE, Wood JD, Rodwell TC, Puria S, Partan SR, Keefe R, Shriver D, Arnason BT, Hart LA (2006) Wild elephants (Loxodonta africana) breeding herds respond to artificially transmitted seismic stimuli. Behav Ecol Sociobiol 59:842–850. https://doi.org/10.1007/s00265-005-0136-2
Patzke N, Kaswera C, Gilissen E, Ihunwo AO, Manger PR (2013) Adult neurogenesis in a giant otter shrew (Potamogale velox). Neuroscience 238:270–279. https://doi.org/10.1016/j.neuroscience.2013.02.025
Patzke N, Olaleye O, Haagensen M, Hof PR, Ihunwo AO, Manger PR (2014a) Organization and chemical neuroanatomy of the African elephant (Loxodonta africana) hippocampus. Brain Struct Funct 219:1587–1601. https://doi.org/10.1007/s00429-013-0587-6
Patzke N, LeRoy A, Ngubane NW, Bennett NC, Medger K, Gravett N, Kaswera-Kyamakya C, Gilissen E, Chawana R, Manger PR (2014b) The distribution of doublecortin-immunopositive cells in the brains of four Afrotherian mammals: the Hottentot golden mole (Amblysomus hottentotus), the rock hyrax (Procavia capensis), the eastern rock sengi (Elephantulus myurus) and the four-toed sengi (Petrodromus tetradactylus). Brain Behav Evol 84:227–241. https://doi.org/10.1159/000367934
Patzke N, Spocter MA, Karlsson KÆ, Bertelsen M, Haagensen M, Chawana R, Streicher S, Kaswera C, Gilissen E, Alagaili AN, Mohammed OB, Reep RL, Bennett NC, Siegel JM, Ihunwo AO, Manger PR (2015) In contrast to many other mammals, cetaceans have relatively small hippocampi that appear to lack adult neurogenesis. Brain Struct Funct 220:361–383. https://doi.org/10.1007/s00429-013-0660-1
Paxinos G, Watson C (2005) The Rat Brain in Stereotaxic Coordinates. Elsevier, Academic Press, New York
Pitkänen A, Savander V, LeDoux JE (1997) Organization of intra-amygdaloid circuitry in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 20:517–523. https://doi.org/10.1016/S0166-2236(97)01125-9
Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. Ann N Y Acad Sci 911:369–391. https://doi.org/10.1111/j.1749-6632.2000.tb06738.x
Plotnik JM, de Waal FBM (2014) Asian elephants (Elephas maximus) reassure others in distress. PeerJ 2:e278. https://doi.org/10.7717/peerj.278
Price JL, Russchen FT, Amaral DG (1987) The limbic region. II. The amygdaloid complex. In: Bjorklund A, Hokfelt T, Swanson LW (eds) Handbook of chemical neuroanatomy, Volume 5, Integrated systems of the CNS, Part 1. Elsevier Science, Amsterdam, pp 279–381
Ramachandran VS, Hubbard EM (2001) Synesthesia: a window into perception, thought, and language. J Conscious Studies 8:3–34
Rasia-Filho AA, Londero RG, Achaval M (1999) Functional activities of the amygdala: an overview. J Psychiat Neuro 25:14–23
Rasmussem LEL, Munger BL (1996) The sensori-neural specializations of the trunk tip (finger) of the Asian elephant, Elephas maximus. Anat Rec 246:127–134. https://doi.org/10.1002/(SICI)1097-0185(199609)
Rasmussen LEL, Lazar J, Greenwood DR (2003) Olfactory adventures of elephantine pheromones. Biochem Soc Trans 31:137–141. https://doi.org/10.1042/bst0310137
Rasmussen LEL, Krishnamurthy V, Sukumar R (2005) Behavioural and chemical confirmation of the preovulatory pheromone, (Z)-7-dodecenyl acetate, in wild Asian elephants: its relationship to musth. Behaviour 142:351–396. https://doi.org/10.1163/1568539053778300
Rolls ET (1999) The brain and emotion. Oxford University Press, Oxford
Romanski LM, Clugnet MC, Bordi F, LeDoux JE (1993) Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav Neurosci 107:444–450. https://doi.org/10.1037//0735-7044.107.3.444
Sah P, Faber ESL, Lopez de Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834. https://doi.org/10.1152/physrev.00002.2003
Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470. https://doi.org/10.1038/nature09817
Saul ML, Helmreich DL, Rehman S, Fudge JL (2014) Proliferating cells in the adolescent rat amygdala: characterization and response to stress. Neuroscience 311:105–117. https://doi.org/10.1016/j.neuroscience.2015.10.003
Saul ML, Helmreich DL, Callahan LM, Fudge JL (2015) Differences in amygdala cell proliferation between adolescent and young adult rats. Dev Psychobiol 56:517–528. https://doi.org/10.1002/dev.21115
Shapiro LA, Ng KL, Kinyamu R, Whitaker-Azmitia P, Geisert EE, Blurton-Jones M, Zhou QY, Ribak CE (2007) Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex. Brain Struct Funct 212:133–148. https://doi.org/10.1007/s00429-007-0151-3
Shoshani J, Kupsky WJ, Marchant GH (2006) Elephant brain part I: gross morphology, functions, comparative anatomy, and evolution. Brain Res Bull 70:124–157. https://doi.org/10.1016/j.brainresbull.2006.03.016
Silver WH, Finger TE (1991) The trigeminal system. In: Snow JB, Getchell TV, Bartoskuk LM, Doty RL (eds) Smell and taste in health and disease. Raven Press, New York, pp 97–108
Soltis J, Blowers TE, Savage A (2011) Measuring positive and negative affect in the voiced sounds of African elephants (Loxodonta africana). J Acoust Soc Am 129:1059–1066. https://doi.org/10.1121/1.3531798
Soltis J, King LE, Douglas-Hamilton I, Vollrath F, Savage A (2014) African elephant alarm calls distinguish between threats from humans and bees. PLoS One 9:e89403. https://doi.org/10.1371/journal.pone.0089403
Stevenson RJ, Attuquayefio T (2013) Human olfactory consciousness and cognition: its unusual features may not result from unusual functions but from limited neocortical processing resources. Front Psychol 4:819. https://doi.org/10.3389/fpsyg.2013.00819
Suárez R, Fernández-Aburto P, Manger PR, Mpodozis J (2011) Deterioration of the Gαo vomeronasal pathway in sexually dimorphic mammals. PLoS One 6:e26436. https://doi.org/10.1371/journal.pone.0026436
Treves A, Tashiro A, Witter MP, Moser EI (2008) What is the mammalian dentate gyrus good for? Neuroscience 154:1155–1172. https://doi.org/10.1016/j.neuroscience.2008.04.073
Turney P, Whitley D, Anderson RW (1996) Evolution, learning and instinct: 100 years of the Baldwin effect. Evol Computation 4:iv–viii. https://doi.org/10.1162/evco.1996.4.3.iv
Vidya TNC, Sukumar R (2005) Social and reproductive behaviour in elephant. Curr Sci 89:1200–1207
Zhang XM, Cai Y, Chu Y, Chen EY, Feng JC, Luo XG, Xiong K, Struble RG, Clough RW, Patrylo PR, Kordower JH, Yan XX (2009) Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat 3:17. https://doi.org/10.3389/neuro.05.017.2009
Acknowledgements
This work was supported by funding from the South African National Research Foundation (BCM and PRM). We thank the relevant wildlife authorities for permission to collect the material used.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no conflict of interest.
Ethical statement
The brains of two African elephants (Loxodonta africana) were used for the purpose of this study. The specimens were obtained in Zimbabwe under the permission of the Zimbabwe Parks and Wildlife Management Authority as well as the Malilangwe Nature Conservation Trust (specimen preparation, treatment and storage described in Manger et al. 2009). The animals were treated and used according to the guidelines of the University of the Witwatersrand Animal Ethics Committee (Clearance number: 2008/36/1).
Rights and permissions
About this article
Cite this article
Limacher-Burrell, A., Bhagwandin, A., Maseko, B.C. et al. Nuclear organization of the African elephant (Loxodonta africana) amygdaloid complex: an unusual mammalian amygdala. Brain Struct Funct 223, 1191–1216 (2018). https://doi.org/10.1007/s00429-017-1555-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-017-1555-3