Individual variation in how animals react to stress and environmental change has become a central topic in a wide range of biological disciplines, from evolutionary ecology to biomedicine. Such variation manifests phenotypically as correlated trait-clusters (referred to as coping styles, behavioral syndromes, shyness-boldness, or personality traits). Thresholds for switching from active coping (fight-flight) to inhibition and passive behavior when exposed to stress depend on experience and genetic factors. Comparative research has revealed a range of neuroendocrine-behavioral associations which are conserved throughout the vertebrate subphylum, including factors affecting perception, learning, and memory of stimuli and events. Here we review conserved aspects of the contribution of neurogenesis and other aspects of neural plasticity to stress coping. In teleost fish, brain cell proliferation and neurogenesis have received recent attention. This work reveals that brain cell proliferation and neurogenesis are associated with heritable variation in stress coping style, and they are also differentially affected by short- and long-term stress in a biphasic manner. Routine-dependent and inflexible behavior in proactive individuals is associated with limited neural plasticity. These evolutionarily conserved relationships hold the potential to illuminate the biological background for stress-related neurobiological disorders.

1.
Aimone JB, Deng W, Gage FH (2010): Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci 14:325-337.
2.
Aimone JB, Li Y, Lee SW, Clemenson GD, Deng W, Gage FH (2014): Regulation and function of adult neurogenesis: from genes to cognition. Physiol Rev 94:991-1026.
3.
Aimone JB, Wiles J, Gage FH (2006): Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9:723-727.
4.
Altman J, Das GD (1965): Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
5.
Ambrogini P, Lattanzi D, Ciuffoli S, Agostini D, Bertini L, Stocchi V, Santi S, Cuppini R (2004): Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 1017:21-31.
6.
Balthazart J, Ball GF (2016): Endocrine and social regulation of adult neurogenesis in songbirds. Front Neuroendocrinol DOI: 10.1016/j.yfrne.2016.03.003.
7.
Benus R, Den Daas S, Koolhaas J, Van Oortmerssen G (1990): Routine formation and flexibility in social and non-social behavior of aggressive and non-aggressive male mice. Behavior 112:176-193.
8.
Bolhuis JE, Schouten WG, De Leeuw JA, Schrama JW, Wiegant VM (2004): Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav Brain Res 152:351-360.
9.
Broglio C, Rodríguez F, Gómez A, Arias J, Salas C (2010): Selective involvement of the goldfish lateral pallium in spatial memory. Behav Brain Res 210:191-201.
10.
Burghardt NS, Park EH, Hen R, Fenton AA (2012): Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 22:1795-1808.
11.
Burns JG, Saravanan A, Rodd H (2009): Rearing environment affects the brain size of guppies: lab-reared guppies have smaller brains than wild-caught guppies. Ethology 115:122-133.
12.
Cameron HA, Glover LR (2015): Adult neurogenesis: beyond learning and memory. Annu Rev Psychol 66:53-81.
13.
Cameron HA, Gould E (1994): Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
14.
Cameron H, Woolley C, McEwen B, Gould E (1993): Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
15.
Carpenter RE, Summers CH (2009): Learning strategies during fear conditioning. Neurobiol Learn Mem 91:415-423.
16.
Castanheira MF, Conceição LE, Millot S, Rey S, Bégout ML, Damsgård B, Kristiansen T, Höglund E, Øverli Ø, Martins CI (2015): Coping styles in farmed fish: consequences for aquaculture. Rev Aquac 7:1-19.
17.
Clint SC, Zupanc GK (2001): Neuronal regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: guidance of migrating young cells by radial glia. Dev Brain Res 130:15-23.
18.
Conrad JL, Weinersmith KL, Brodin T, Saltz J, Sih A (2011): Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395-435.
19.
Coppens CM, De Boer SF, Koolhaas JM (2010): Coping styles and behavioural flexibility: towards underlying mechanisms. Philos Trans R Soc Lond B Biol Sci 365:4021-4028.
20.
Corwin JT (1981): Postembryonic production and aging of inner ear hair cells in sharks. J Comp Neurol 201:541-553.
21.
Crawford DL, Oleksiak MF (2007): The biological importance of measuring individual variation. J Exp Biol 210:1613-1621.
22.
Demski LS (2013): The pallium and mind/behavior relationships in teleost fishes. Brain Behav Evol 82:31-44.
23.
Deng W, Aimone JB, Gage FH (2010): New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339-350.
24.
Dingemanse NJ, Wolf M (2010): Recent models for adaptive personality differences: a review. Philos Trans R Soc Lond B Biol Sci 365:3947-3958.
25.
Dunlap KD, Castellano JF, Prendaj E (2006): Social interaction and cortisol treatment increase cell addition and radial glia fiber density in the diencephalic periventricular zone of adult electric fish, Apteronotus leptorhynchus. Horm Behav 50:10-17.
26.
Dunlap KD, Chung M, Castellano JF (2013): Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish. J Exp Biol 216:2434-2441.
27.
Dunlap KD, Mccarthy EA, Jashari D (2008): Electrocommunication signals alone are sufficient to increase neurogenesis in the brain of adult electric fish, Apteronotus leptorhynchus. Dev Neurobiol 68:1420-1428.
28.
Dunlap KD, Tran A, Ragazzi MA, Krahe R, Salazar VL (2016): Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis. Proc R Soc Lond B Biol Sci 283:20152113.
29.
Ekström P, Johnsson CM, Ohlin LM (2001): Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration (secondary matrix) zones. J Comp Neurol 436:92-110.
30.
Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn A-M, Nordborg C, Peterson DA, Gage FH (1998): Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
31.
Faigle R, Song H (2013): Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta 1830:2435-2448.
32.
Ferragud A, Haro A, Sylvain A, Velazquez-Sanchez C, Hernandez-Rabaza V, Canales J (2010): Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress. Behav Brain Res 210:134-139.
33.
Gosling SD (2001): From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45.
34.
Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997): Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498.
35.
Gould E, Tanapat P (1999): Stress and hippocampal neurogenesis. Biol Psychiatry 46:1472-1479.
36.
Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006): Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263-277.
37.
Hau M, Goymann W (2015): Endocrine mechanisms, behavioral phenotypes and plasticity: known relationships and open questions. Front Zool 12:1-15.
38.
Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ (2004): Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 19:131-144.
39.
Herczeg G, Gonda A, Balázs G, Noreikiene K, Merilä J (2015): Experimental evidence for sex-specific plasticity in adult brain. Front Zool 12:1.
40.
Hinsch K, Zupanc G (2007): Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis. Neuroscience 146:679-696.
41.
Johansen IB, Sørensen C, Sandvik GK, Nilsson GE, Höglund E, Bakken M, Øverli Ø (2012): Neural plasticity is affected by stress and heritable variation in stress coping style. Comp Biochem Physiol Part D Genomics Proteomics 7:161-171.
42.
Johns PR, Easter SS (1977): Growth of the adult goldfish eye. 2. Increase in retinal cell number. J Comp Neurol 176:331-341.
43.
Kaplan MS, Hinds JW (1977): Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-1094.
44.
Kaslin J, Ganz J, Brand M (2008): Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Proc R Soc Lond B Biol Sci 363:101-122.
45.
Kee N, Teixeira CM, Wang AH, Frankland PW (2007): Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355-362.
46.
Kempermann G (2015): Activity-based maintenance of adult hippocampal neurogenesis: maintaining a potential for lifelong plasticity; in Kuhn HG, Eisch AJ (ed): Neural Stem Cells in Development, Adulthood and Disease. New York, Springer, pp 119-123.
47.
Kempermann G, Song H, Gage FH (2015): Neurogenesis in the adult hippocampus. Cold Spring Harb Perspect Biol 7:a018812.
48.
Kim JJ, Diamond DM (2002): The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453-462.
49.
Kirby ED, Muroy SE, Sun WG, Covarrubias D, Leong MJ, Barchas LA, Kaufer D (2013): Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. Elife 2:e00362.
50.
Koolhaas J, De Boer S, Coppens C, Buwalda B (2010): Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307-321.
51.
Koolhaas J, Korte S, De Boer S, Van Der Vegt B, Van Reenen C, Hopster H, De Jong I, Ruis M, Blokhuis H (1999): Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925-935.
52.
Korte SM, Koolhaas JM, Wingfield JC, Mcewen BS (2005): The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev 29:3-38.
53.
Kotrschal A, Rogell B, Maklakov AA, Kolm N (2012): Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata. Behav Ecol Sociobiol 66:1485-1492.
54.
Kropff E, Yang SM, Schinder AF (2015): Dynamic role of adult-born dentate granule cells in memory processing. Curr Opin Neurobiol 35:21-26.
55.
Kuroyanagi Y, Okuyama T, Suehiro Y, Imada H, Shimada A, Naruse K, Takeda H, Kubo T, Takeuchi H (2010): Proliferation zones in adult medaka (Oryzias latipes) brain. Brain Res 1323:33-40.
56.
Lagace DC, Donovan MH, Decarolis NA, Farnbauch LA, Malhotra S, Berton O, Nestler EJ, Krishnan V, Eisch AJ (2010): Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc Natl Acad Sci USA 107:4436-4441.
57.
Leyhausen C, Kirschbaum F, Szabo T, Erdelen M (1987): Differential growth in the brain of the weakly electric fish, Apteronotus leptorhynchus (Gymnotiformes), during ontogenesis. Part 1 of 2. Brain Behav Evol 30:230-238.
58.
Mackenzie S, Ribas L, Pilarczyk M, Capdevila DM, Kadri S, Huntingford FA (2009): Screening for coping style increases the power of gene expression studies. PLoS One 4:e5314.
59.
Marín-Burgin A, Mongiat LA, Pardi MB, Schinder AF (2012): Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335:1238-1242.
60.
Maruska KP, Carpenter RE, Fernald RD (2012): Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status. J Comp Neurol 520:3471-3491.
61.
Ming G-L, Song H (2011): Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702.
62.
Moreira P, Pulman KG, Pottinger TG (2004): Extinction of a conditioned response in rainbow trout selected for high or low responsiveness to stress. Horm Behav 46:450-457.
63.
Northcutt RG (2006): Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494:903-943.
64.
Nottebohm F (2002): Neuronal replacement in adult brain. Brain Res Bull 57:737-749.
65.
Opendak M, Gould E (2015): Adult neurogenesis: a substrate for experience-dependent change. Trends Cogn Sci 19:151-161.
66.
Ott R, Zupanc GK, Horschke I (1997): Long-term survival of postembryonically born cells in the cerebellum of gymnotiform fish, Apteronotus leptorhynchus. Neurosci Lett 221:185-188.
67.
Øverli Ø, Sørensen C, Pulman KG, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007): Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396-412.
68.
Øverli Ø, Winberg S, Pottinger TG (2005): Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout - a review. Int Comp Biol 45:463-474.
69.
Parihar VK, Hattiangady B, Kuruba R, Shuai B, Shetty AK (2011): Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol Psychiatr 16:171-183.
70.
Peretto P, Bonfanti L (2015): Adult neurogenesis 20 years later: physiological function vs brain repair. Front Neurosci 9:71.
71.
Pottinger T, Carrick T (1999): Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122-132.
72.
Publisi-Allegra S, Andolina D (2015): Serotonin and stress coping. Behav Brain Res 277:58-67.
73.
Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA (2006): Integration of new neurons into functional neural networks. J Neurosci 26:12237-12241.
74.
Réale D, Reader SM, Sol D, Mcdougall PT, Dingemanse NJ (2007): Integrating animal temperament within ecology and evolution. Biol Rev 82:291-318.
75.
Rey S, Ribas L, Morera Capdevila D, Callol A, Huntingford FA, Pilarczyk M, Kadri S, Mackenzie S (2016): Differential responses to environmental challenge by common carp Cyprinus carpio highlight the importance of coping style in integrative physiology. J Fish Biol 88:1056-1059.
76.
Rodriguez F, López J, Vargas J, Broglio C, Gómez Y, Salas C (2002): Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish. Brain Res Bull 57:499-503.
77.
Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N (2006): Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850-1856.
78.
Rowlerson A, Veggetti A (2001): Cellular mechanisms of post-embryonic muscle growth in aquaculture species. Fish Physiol 18:103-140.
79.
Ruiz-Gomez ML, Huntingford FA, Øverli Ø, Thörnqvist P-O, Höglund E (2011): Response to environmental change in rainbow trout selected for divergent stress coping styles. Physiol Behav 102:317-322.
80.
Salvanes AGV, Moberg O, Ebbesson LO, Nilsen TO, Jensen KH, Braithwaite VA (2013): Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc Lond B Biol Sci 280:20131331.
81.
Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S (2005): Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 192:348-356.
82.
Schjolden J, Pulman KG, Pottinger TG, Tottmar O, Winberg S (2006): Serotonergic characteristics of rainbow trout divergent in stress responsiveness. Physiol Behav 87:938-947.
83.
Schmidt-Hieber C, Jonas P, Bischofberger J (2004): Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
84.
Schoenfeld TJ, Cameron HA (2015): Adult neurogenesis and mental illness. Neuropsychopharmacology 40:113-128.
85.
Sih A, Bell A, Johnson JC (2004a): Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evolut 19:372-378.
86.
Sih A, Bell AM, Johnson JC, Ziemba RE (2004b): Behavioral syndromes: an integrative overview. Q Rev Biol 79:241-277.
87.
Sih A, Mathot KJ, Moirón M, Montiglio P-O, Wolf M, Dingemanse NJ (2015): Animal personality and state-behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50-60.
88.
Sîrbulescu RF, Zupanc GK (2013): Neuronal regeneration; in Evans DH, Claiborne JB, Currie S (eds): The Physiology of Fishes. Boca Raton, CRC Press, pp 405-441.
89.
Skaggs K, Goldman D, Parent JM (2014): Excitotoxic brain injury in adult zebrafish stimulates neurogenesis and long-distance neuronal integration. Glia 62:2061-2079.
90.
Sneddon L (2003): The bold and the shy: individual differences in rainbow trout. J Fish Biol 62:971-975.
91.
Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA (2011): Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476:458-461.
92.
Sørensen C, Bohlin LC, Øverli Ø, Nilsson GE (2011): Cortisol reduces cell proliferation in the telencephalon of rainbow trout (Oncorhynchus mykiss). Physiol Behav 102:518-523.
93.
Sørensen C, Johansen IB, Øverli Ø (2013): Neural plasticity and stress coping in teleost fishes. Gen Comp Endocrinol 181:25-34.
94.
Sørensen C, Nilsson GE, Summers CH, Øverli Ø (2012): Social stress reduces forebrain cell proliferation in rainbow trout (Oncorhynchus mykiss). Behav Brain Res 227:311-318.
95.
Stamps J, Groothuis TG (2010): The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301-325.
96.
Van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002): Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
97.
Vargas JP, López JC, Portavella M (2009): What are the functions of fish brain pallium? Brain Res Bull 79:436-440.
98.
Veenema AH, Koolhaas JM, Kloet ER (2004): Basal and stress-induced differences in HPA axis, 5-HT responsiveness, and hippocampal cell proliferation in two mouse lines. Ann NY Acad Sci 1018:255-265.
99.
Verbeek MEM, Drent PJ, Wiepkema PR (1994): Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113-1121.
100.
Vindas M, Johansen I, Folkedal O, Höglund E, Gorissen M, Flik G, Kristiansen T, Øverli Ø (2016): Brain serotonergic activation in growth-stunted farmed salmon: adaption vs pathology. R Soc Open Sci 3:160030.
101.
Von Krogh K, Sørensen C, Nilsson GE, Øverli Ø (2010): Forebrain cell proliferation, behavior, and physiology of zebrafish, Danio rerio, kept in enriched or barren environments. Physiol Behav 101:32-39.
102.
Wang S, Scott BW, Wojtowicz JM (2000): Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257.
103.
Warner-Schmidt JL, Duman RS (2006): Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16:239-249.
104.
Weatherley A, Gill H (1985): Dynamics of increase in muscle fibers in fishes in relation to size and growth. Experientia 41:353-354.
105.
Wilson DS, Clark AB, Coleman K, Dearstyne T (1994): Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442-446.
106.
Wingfield JC (2003): Control of behavioural strategies for capricious environments. Anim Behav 66:807-816.
107.
Wiskott L, Rasch MJ, Kempermann G (2006): A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 16:329-343.
108.
Wong RY, Lamm MS, Godwin J (2015): Characterizing the neurotranscriptomic states in alternative stress coping styles. BMC Genomics 16:425.
109.
Zakon HH (1984): Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age. J Comp Neurol 228:557-570.
110.
Zozulya AA, Gabaeva MV, Sokolov OY, Surkina ID, Kost NV (2008): Personality, coping style, and constitutional neuroimmunology. J Immunotoxicol 5:221-225.
111.
Zupanc G (2001): Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav Evol 58:250-275.
112.
Zupanc GK (2008a): Adult neurogenesis and neuronal regeneration in the brain of teleost fish. J Physiol Paris 102:357-373.
113.
Zupanc GK (2008b): Adult neurogenesis in teleost fish. Cold Spring Harb Monogr Arch 52:571-592.
114.
Zupanc GK, Hinsch K, Gage FH (2005): Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488:290-319.
115.
Zupanc GK, Horschke I (1995): Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J Comp Neurol 353:213-233.
116.
Zupanc GK, Horschke I, Ott R, Rascher GB (1996): Postembryonic development of the cerebellum in gymnotiform fish. J Comp Neurol 370:443-464.
117.
Zupanc GK, Ott R (1999): Cell proliferation after lesions in the cerebellum of adult teleost fish: time course, origin, and type of new cells produced. Exp Neurol 160:78-87.
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