Species diversity in experimental neuroscience research provides a vital resource. Addressing contemporary questions using nontraditional model systems (i.e., studies of species other than rats or mice) have regularly led to serendipitous breakthroughs in this discipline. The “comparative” approach to neuroscience and neuroendocrinology harnesses the diversity of organisms—and their nervous systems—that have been refined and differentiated over evolutionary timescales. Here, we review some recent examples of unexpected and impactful outcomes resulting from research on nontraditional study species. This work shows that maintaining broad diversity in study species will continue to provide the best path forward for extraordinary advances and insights into the neural mechanisms of behavior.
AarssenL. (2013). Valuation branding for bioscience research in the twenty first century. BioScience, 63, 417-418.
2.
AbbassiP.BurleyN. T. (2012). Nice guys finish last: Same-sex sexual behavior and pairing success in male budgerigars. Behavioral Ecology, 23, 775-782. doi:10.1093/beheco/ars030
3.
AltmanJ.DasG. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. The Journal of Comparative Neurology, 124, 319-335. doi:10.1002/cne.901240303
4.
AnackerA. M.BeeryA. K. (2013). Life in groups: The roles of oxytocin in mammalian sociality. Frontiers in Behavioral Neuroscience, 7, 185. doi:10.3389/fnbeh.2013.00185
5.
AnagnostouE.SooryaL.BrianJ.DupuisA.MankadD.SmileS.JacobS. (2014). Intranasal oxytocin in the treatment of autism spectrum disorders: A review of literature and early safety and efficacy data in youth. Brain Research, 1580, 188-198. doi:10.1016/j.brainres.2014.01.049
6.
BarneaA.NottebohmF. (1994). Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proceedings of the National Academy of Sciences of the United States of America, 91, 11217-11221.
7.
BeeryA. K.ZuckerI. (2010). Oxytocin and same-sex social behavior in female meadow voles. Neuroscience, 169, 665-673. doi:10.1016/j.neuroscience.2010.05.023
8.
BlausteinJ. D. (1992). Cytoplasmic estrogen receptors in rat brain: Immunocytochemical evidence using three antibodies with distinct epitopes. Endocrinology, 131, 1336-1342.
9.
BrennanP. L. R.IrschickD. J.JohnsonN.AlbertsonR. C. (2014). Oddball science: Why studies of unusual evolutionary phenomena are crucial. Bioscience, 64, 178-179. doi:10.1093/biosci/bit039
10.
BrenowitzE. A.ZakonH. H. (2015). Emerging from the bottleneck: Benefits of the comparative approach to modern neuroscience. Trends in Neurosciences, 38, 273-278. doi:10.1016/j.tins.2015.02.008
11.
CarlsonB. A. (2012). Diversity matters: The importance of comparative studies and the potential for synergy between neuroscience and evolutionary biology. Archives of Neurology, 69, 987-993. doi:10.1001/archneurol.2012.77
12.
CostaB.PiniS.GabelloniP.AbelliM.LariL.CardiniA.. . . MartiniC. (2009). Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology, 34, 1506-1514. doi:10.1016/j.psyneuen.2009.05.006
13.
DaddsM. R.MacDonaldE.CauchiA.WilliamsK.LevyF.BrennanJ. (2014). Nasal oxytocin for social deficits in childhood autism: A randomized controlled trial. Journal of Autism and Developmental Disorders, 44(3), 521-531. doi:10.1007/s10803-013-1899-3
14.
EdelsteinR. S.van AndersS. M.ChopikW. J.GoldeyK. L.WardeckerB. M. (2014). Dyadic associations between testosterone and relationship quality in couples. Hormones and Behavior, 65, 401-407. doi:10.1016/j.yhbeh.2014.03.003
15.
ElieJ. E.MathevonN.VignalC. (2011). Same-sex pair-bonds are equivalent to male–female bonds in a life-long socially monogamous songbird. Behavioral Ecology and Sociobiology, 65, 2197-2208. doi:10.1007/s00265-011-1228-9
16.
FilardoE. J.QuinnJ. A.BlandK. I.FrackeltonA. R.Jr. (2000). Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Molecular Endocrinology, 14, 1649-1660. doi:10.1210/mend.14.10.0532
17.
FlexnerA. (1939). The usefulness of useless knowledge. Princeton, NJ: Princeton University Press.
18.
GeistV. (1974). Mountain sheep: A study in behaviour and evolution. The Quarterly Review of Biology, 49, 168-169. doi:10.1086/408061
19.
GervainJ.VinesB. W.ChenL. M.SeoR. J.HenschT. K.WerkerJ. F.YoungA. H. (2013). Valproate reopens critical-period learning of absolute pitch. Frontiers in Systems Neuroscience, 7, 102. doi:10.3389/fnsys.2013.00102
20.
GodwinJ.CrewsD. (1999). Hormonal regulation of progesterone receptor mRNA expression in the hypothalamus of whiptail lizards: Regional and species differences. Journal of Neurobiology, 39, 287-293.
21.
GoldmanS. A.NottebohmF. (1983). Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proceedings of the National Academy of Sciences of the United States of America, 80, 2390-2394.
22.
GorskiR. A.GordonJ. H.ShryneJ. E.SouthamA. M. (1978). Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Research, 148, 333-346.
23.
GouldE. (2007). How widespread is adult neurogenesis in mammals?Nature Reviews Neuroscience, 8, 481-488. doi:10.1038/nrn2147
24.
Gruder-AdamsS.GetzL. L. (1985). Comparison of the mating system and paternal behavior in Microtus-ochrogaster and Microtus-pennsylvanicus. Journal of Mammalogy, 66, 165-167. doi:10.2307/1380976
25.
HartlineH. K.WagnerH. G.RatliffF. (1956). Inhibition in the eye of Limulus. Journal of General Psychology, 5, 651-671.
26.
HenschT. K. (2004). Critical period regulation. Annual Review of Neuroscience, 27, 549-579. doi:10.1146/annurev.neuro.27.070203.144327
27.
HenschT. K.BilimoriaP. M. (2012). Re-opening windows: Manipulating critical periods for brain development. Cerebrum: The Dana Forum on Brain Science, 2012, 1-18.
28.
HoekzemaE.SchagenS. E.KreukelsB. P.VeltmanD. J.Cohen-KettenisP. T.Delemarre-vandeWaalH.BakkerJ. (2015). Regional volumes and spatial volumetric distribution of gray matter in the gender dysphoric brain. Psychoneuroendocrinology, 55, 59-71. doi:10.1016/j.psyneuen.2015.01.016
29.
HubelD. H.WieselT. N.LeVayS. (1976). Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Spring Harbor Symposia on Quantitative Biology, 40, 581-589.
30.
InselT. R.O’BrienD. J.LeckmanJ. F. (1999). Oxytocin, vasopressin, and autism: Is there a connection?Biological Psychiatry, 45, 145-157.
31.
InselT. R.ShapiroL. E. (1992). Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proceedings of the National Academy of Sciences of the United States of America, 89, 5981-5985.
32.
InselT. R.WangZ. X.FerrisC. F. (1994). Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. Journal of Neuroscience, 14, 5381-5392.
33.
KellyM. J.MossR. L.DudleyC. A. (1976). Differential sensitivity of preoptic-septal neurons to microelectrophoresed estrogen during the estrous cycle. Brain Research, 114, 152-157.
34.
KnudsenE. I. (2004). Sensitive periods in the development of the brain and behavior. Journal of Cognitive Neuroscience, 16, 1412-1425. doi:10.1162/0898929042304796
35.
KsendzovskyA.PomeraniecI. J.ZaghloulK. A.ProvencioJ. J.ProvencioI. (2017). Clinical implications of the melanopsin-based non-image-forming visual system. Neurology, 88, 1282-1290. doi:10.1212/WNL.0000000000003761
36.
LimM. M.WangZ.OlazabalD. E.RenX.TerwilligerE. F.YoungL. J. (2004). Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature, 429, 754-757. doi:10.1038/nature02539
37.
LimM. M.YoungL. J. (2004). Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience, 125, 35-45. doi:10.1016/j.neuroscience.2003.12.008
38.
LimM. M.YoungL. J. (2006). Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Hormones and Behavior, 50, 506-517. doi:10.1016/j.yhbeh.2006.06.028
39.
LiuX.WangC. A.ChenY.-Z. (1995). Nongenomic effect of glucocorticoid on the release of arginine vasopressin from hypothalamic slices in rats. Neuroendocrinology, 62, 628-633. doi:10.1159/000127059
40.
LorenzK. (1935). Der Kumpan in der Umwelt des Vogels [The companion in the environment of the bird]. Journal Für Ornithologie, 83, 289-413. doi:10.1007/bf01905572
41.
MangerP. R.CortJ.EbrahimN.GoodmanA.HenningJ.KaroliaM.. . . StrkaljG. (2008). Is 21st century neuroscience too focussed on the rat/mouse model of brain function and dysfunction?Frontiers in Neuroanatomy, 2, 5. doi:10.3389/neuro.05.005.2008
42.
MarderE. (2002). Non-mammalian models for studying neural development and function. Nature, 417, 318-321. doi:10.1038/417318a
43.
MirtoA. J.AustinK. J.UthlautV. A.RoselliC. E.AlexanderB. M. (2017). Fos expression in the olfactory pathway of high- and low-sexually performing rams exposed to urine from estrous or ovariectomized ewes. Applied Animal Behaviour Science, 186, 22-28. doi:10.1016/j.applanim.2015.09.001
44.
MooreF. L.MillerL. J. (1984). Stress-induced inhibition of sexual behavior: Corticosterone inhibits courtship behaviors of a male amphibian (Taricha Granulosa). Hormones and Behavior, 18, 400-410. doi:10.1016/0018-506X(84)90026-6
45.
MooreM. C.CrewsD. (1986). Sex steroid hormones in natural populations of a sexual whiptail lizard Cnemidophorus inornatus, a direct evolutionary ancestor of a unisexual parthenogen. General and Comparative Endocrinology, 63, 424-430.
46.
MooreM. C.WhittierJ. M.CrewsD. (1985). Sex steroid hormones during the ovarian cycle of an all-female, parthenogenetic lizard and their correlation with pseudosexual behavior. General and Comparative Endocrinology, 60, 144-153.
47.
MundayP. L.BustonP. M.WarnerR. R. (2006). Diversity and flexibility of sex-change strategies in animals. Trends in Ecology & Evolution, 21, 89-95. doi:10.1016/j.tree.2005.10.020
48.
NottebohmF.ArnoldA. P. (1976). Sexual dimorphism in vocal control areas of the songbird brain. Science, 194, 211-213.
49.
OrchinikM.MurrayT.MooreF. (1991). A corticosteroid receptor in neuronal membranes. Science, 252, 1848-1851. doi:10.1126/science.2063198
50.
OwmanC.BlayP.NilssonC.LolaitS. J. (1996). Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt’s lymphoma and widely distributed in brain and peripheral tissues. Biochemical and Biophysical Research Communications, 228, 285-292. doi:10.1006/bbrc.1996.1654
51.
PackardM. G.KohlmaierJ. R.AlexanderG. M. (1996). Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: Interaction with cholinergic systems. Behavioral Neuroscience, 110, 626-632.
52.
PackardM. G.TeatherL. A. (1997). Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport, 8, 3009-3013. doi:10.1097/00001756-199709290-00004
53.
PietrasR. J.SzegoC. M. (1977). Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature, 265, 69-72. doi:10.1038/265069a0
54.
ProvencioI.JiangG.De GripW. J.HayesW. P.RollagM. D. (1998). Melanopsin: An opsin in melanophores, brain, and eye. Proceedings of the National Academy of Sciences of the United States of America, 95, 340-345.
55.
RaismanG.FieldP. M. (1971). Sexual dimorphism in the preoptic area of the rat. Science, 173, 731-733.
56.
RevankarC. M.CiminoD. F.SklarL. A.ArterburnJ. B.ProssnitzE. R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science, 307, 1625-1630.
57.
RoeckleinK. A.RohanK. J.DuncanW. C.RollagM. D.RosenthalN. E.LipskyR. H.ProvencioI. (2009). A missense variant (P10L) of the melanopsin (OPN4) gene in seasonal affective disorder. Journal of Affective Disorders, 114, 279-285. doi:10.1016/j.jad.2008.08.005
58.
RoselliC. E.LarkinK.ReskoJ. A.StellflugJ. N.StormshakF. (2004). The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference. Endocrinology, 145, 478-483. doi:10.1210/en.2003-1098
59.
RoselliC. E.ReddyR. C.KaufmanK. R. (2011). The development of male-oriented behavior in rams. Frontiers in Neuroendocrinology, 32, 164-169. doi:10.1016/j.yfrne.2010.12.007
60.
SatoS. M.WoolleyC. S. (2016). Acute inhibition of neurosteroid estrogen synthesis suppresses status epilepticus in an animal model. eLife, 5. doi:10.7554/eLife.12917
61.
SzegoC. M.DavisJ. S. (1967). Adenosine 3’,5’-monophosphate in rat uterus: Acute elevation by estrogen. Proceedings of the National Academy of Sciences of the United States of America, 58, 1711-1718.
62.
TomaszyckiM. L.ZatirkaB. P. (2014). Same-sex partner preference in zebra finches: Pairing flexibility and choice. Archives of Sexual Behavior, 43, 1469-1475. doi:10.1007/s10508-014-0377-0
63.
Toran-AllerandC. D.GuanX.MacLuskyN. J.HorvathT. L.DianoS.SinghM.. . . TinnikovA. A. (2002). ER-X: A novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. Journal of Neuroscience, 22, 8391-8401.
64.
TsutsuiK.BentleyG. E.BedecarratsG.OsugiT.UbukaT.KriegsfeldL. J. (2010). Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Frontiers in Neuroendocrinology, 31, 284-295. doi:10.1016/j.yfrne.2010.03.001
65.
TsutsuiK.SaigohE.UkenaK.TeranishiH.FujisawaY.KikuchiM.. . . SharpP. J. (2000). A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochemical and Biophysical Research Communications, 275, 661-667. doi:10.1006/bbrc.2000.3350
66.
van AndersS. M.GoldeyK. L. (2010). Testosterone and partnering are linked via relationship status for women and “relationship orientation” for men. Hormones and Behavior, 58, 820-826. doi:10.1016/j.yhbeh.2010.08.005
67.
van AndersS. M.HamiltonL. D.WatsonN. V. (2007). Multiple partners are associated with higher testosterone in North American men and women. Hormones and Behavior, 51, 454-459. doi:10.1016/j.yhbeh.2007.01.002
68.
van AndersS. M.WatsonN. V. (2007). Testosterone levels in women and men who are single, in long-distance relationships, or same-city relationships. Hormones and Behavior, 51, 286-291. doi:10.1016/j.yhbeh.2006.11.005
69.
WeikumW. M.OberlanderT. F.HenschT. K.WerkerJ. F. (2012). Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception. Proceedings of the National Academy of Sciences of the United States of America, 109(Suppl. 2), 17221-17227. doi:10.1073/pnas.1121263109
70.
WieselT. N.HubelD. H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology, 26, 1003-1017.
71.
WoolleyC. S.McEwenB. S. (1994). Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. Journal of Neuroscience, 14, 7680-7687.
72.
WoolleyS. C.SakataJ. T.CrewsD. (2004). Tracing the evolution of brain and behavior using two related species of whiptail lizards: Cnemidophorus uniparens and Cnemidophorus inornatus. ILAR Journal, 45, 46-53.
73.
YatawaraC. J.EinfeldS. L.HickieI. B.DavenportT. A.GuastellaA. J. (2016). The effect of oxytocin nasal spray on social interaction deficits observed in young children with autism: A randomized clinical crossover trial. Molecular Psychiatry, 21(9), 1225-1231. doi:10.1038/mp.2015.162
74.
YoungL. J. (1999). Oxytocin and vasopressin receptors and species-typical social behaviors. Hormones and Behavior, 36, 212-221. doi:10.1006/hbeh.1999.1548
75.
YoungL. J.LimM. M.GingrichB.InselT. R. (2001). Cellular mechanisms of social attachment. Hormones and Behavior, 40, 133-138. doi:10.1006/hbeh.2001.1691
76.
YoungL. J.NilsenR.WaymireK. G.MacGregorG. R.InselT. R. (1999). Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature, 400, 766-768. doi:10.1038/23475
77.
Zubiaurre-ElorzaL.JunqueC.Gomez-GilE.GuillamonA. (2014). Effects of cross-sex hormone treatment on cortical thickness in transsexual individuals. Journal of Sexual Medicine, 11, 1248-1261. doi:10.1111/jsm.12491
