© 2002 by The Society for Integrative and Comparative Biology
Cortisol and Pacific Salmon: A New Look at the Role of Stress Hormones in Olfaction and Home-stream Migration1
1 Department of EPO Biology, Campus Box 334, University of Colorado, Boulder, Colorado 80309-0334
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 SYNOPSIS INTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Pacific salmon (genus Oncorhynchus) exhibit an interesting and uncommon life-history pattern that combines semelparity, anadromy, and navigation (homing). During smoltification, young salmon imprint on the chemical composition of their natal stream water (the home-stream olfactory bouquet or "HSOB"); they then migrate to the ocean where they spend a few years feeding prior to migrating back to their natal freshwater stream to spawn. Upstream migration is guided by the amazing ability to discriminate between the chemical compositions of different stream waters and thus identify and travel to their home-stream. Pacific salmon demonstrate marked somatic and neural degeneration changes during home-stream migration and at the spawning grounds. The appearance of these pathologies is correlated with a marked elevation in plasma cortisol levels. While the mechanisms of salmonid homing are not completely understood, it is known that adult salmon continuously utilize two of their primary sensory systems, olfaction and vision, during homing. Olfaction is the primary sensory system involved in freshwater homing and "HSOB" recognition, and will be emphasized here. Previously, we proposed that the increase in plasma cortisol during Pacific salmon home-stream migration is adaptive because it enhances the salmon's ability to recall the imprinted memory of the "HSOB" (Carruth, 1998
; Carruth et al., 2000b). Elevated plasma concentrations of cortisol could prime the hippocampus or other olfactory regions of the brain to recall this memory and, therefore, aid in directing the fish to their natal stream. Thus, specific responses of salmon to stressors could enhance reproductive success. |
INTRODUCTION |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Pacific salmon (genus Oncorhynchus) exhibit an interesting and uncommon life-history pattern that combines navigation, anadromy, and in most species, semelparity. Pacific salmon are anadromous (sea-run) fish that migrate from freshwater to the ocean and then back to freshwater to spawn. In addition, adults of most Pacific salmon species die soon after a single reproductive spawning event (semelparity). After sexual maturation, Pacific salmon navigate (home) to their natal freshwater streams where females select a nest site, and dig a spawning nest in the gravel, and oviposit. Males compete to fertilize eggs, and a week or two after spawning adults of both sexes die.
Kokanee salmon (Oncorhynchus nerka kennerlyi) are a landlocked subspecies of sockeye salmon (O. nerka nerka). This subspecies migrates solely in freshwater between rivers and lakes (Stabell, 1992). As with sockeye salmon, kokanee migrate (home) to the exact stream in which they hatched to spawn and then die (Magnuson, 1996). A generalized life cycle of kokanee salmon is shown in Figure 1. As with all species of Pacific salmon, this upstream migration is guided by the salmon's olfactory system and their amazing ability to discriminate between the chemical compositions of different streams. Kokanee salmon are a good model for studying salmon migration and homing because they return to their natal spawning grounds with a high degree of accuracy (Ueda et al., 1995).
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Young salmon undergo many physiological, morphological and behavioral changes that prepare them for their downstream migration to the ocean as well as for life in salt water. During this period, known as the parr-smolt transformation or smoltification, they imprint on the unique chemical composition of the water at their natal spawning ground (the home-stream olfactory bouquet or "HSOB"). Olfactory imprinting has been correlated with a plasma surge of thyroxine and cortisol (Hasler and Scholz, 1983
; Dickhoff et al., 1990) and is crucial for salmon to return successfully to their natal stream. |
HOMING IN PACIFIC SALMON |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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The mechanisms of salmonid homing are not completely understood, but it is known that adult salmon continuously utilize two of their primary sensory systems, olfaction and vision, during homing (Ueda et al., 1995
; Dittman and Quinn, 1996). Positive rheotaxis, salinity preference, magnetic detection, as well as open-water orientation have all also been suggested to play a role in orientation during home-stream migration in sea-run Pacific salmon (Quinn and Dittman, 1990; Dittman and Quinn, 1996).
Olfaction is the primary sensory system involved in freshwater homing and "HSOB" recognition, and therefore will be the sensory system emphasized here. When salmon imprint on the unique chemical composition of their natal spawning grounds, they are actually imprinting on the individual combination of odorants found in various concentrations in stream water. There are four major aquatic odorants fish recognize: amino acids, bile salts, steroid hormones, and prostaglandins (Hara, 1992a, b) and the olfactory system of salmonids is able to detect very low concentrations of these odorants, but particularly amino acids (10–6 to 10–7; Hara, 1992a, b) and bile salts (10–8 to 10–10; Døving et al., 1980; Hara, 1992a, b).
Electrophysiological studies, conducted since the 1960s, have demonstrated that there is an increase in brain neuronal activity, especially in the olfactory bulbs and posterior cerebellum, in salmon exposed to their home-stream water (Hasler and Scholz, 1983; Hara et al., 1984). Many studies using electrophysiological recordings have shown that Pacific salmon, including kokanee, can distinguish the "HSOB" on which they have imprinted from either natural water samples or synthetic chemicals (Ueda et al., 1967; Hasler and Scholz, 1983).
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PHYSIOLOGICAL AND HISTOLOGICAL CHANGES ASSOCIATED WITH MIGRATION AND SPAWNING |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Pacific salmon demonstrate marked somatic degeneration of all major organ systems including the central nervous system during home-stream migration and at the spawning grounds, and many of these pathologies are similar to those that occur during human aging (Robertson and Wexler, 1960
, 1962a). Senile plaques resembling those associated with human aging and Alzheimer's disease, as well as dead neurons and neurites, have been detected in the brains of spawning kokanee salmon (Maldonado et al., 2000). In addition, the adrenocortical tissue (interrenal cells; homologue of mammalian adrenocortical cells) dispersed within the head kidney exhibits hyperplasia during migration and then degeneration during spawning (Robertson and Wexler, 1959). These "senescent" changes occur in landlocked kokanee as well as ocean-going Pacific salmon (Robertson and Wexler, 1962b).
The onset of degenerative tissue changes during up-stream migration and spawning can be delayed but not prevented (Robertson and Wexler, 1962b; McBride and van Overbeeke, 1969). Therefore, it has been hypothesized that the degenerative changes observed with sexual maturation and migration represent an accelerated aging phenomenon (Robertson and Wexler, 1962a, b) and that sexual maturation and spawning influence, but are not necessary for, the rapid aging process and death (Dickhoff, 1989).
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ACTIVATION OF THE HYPOTHALAMIC-PITUITARY-INTERRENAL AXIS |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Pacific salmon also experience an extreme activation of the hypothalamic-pituitary-adrenal (HPA axis; Fig. 2). Plasma levels of corticosteroid or hormones (glucocorticoids including cortisol, corticosterone and cortisone) peak during migration, with cortisol being the predominant stress hormone (Schmidt and Idler, 1962
; Fagerlund, 1967; Fagerlund et al., 1995). Migrating kokanee salmon experience a comparable elevation in plasma cortisol compared to the levels seen in ocean-run species (Carruth et al., 2000a; Fig. 3). Sexually mature migrating kokanee have a mean plasma cortisol level of 639 ± 55.9 ng/ml up from the 259 ± 71.8 ng/ml mean level observed in sexually immature fish with the plasma cortisol concentration decreasing significantly to a mean of 457 ± 71.8 ng/ml in spawning fish (Carruth et al., 2000a). Cortisol has been implicated in the senescence and ultimately the death of adult Pacific salmon after spawning (Dickhoff, 1989). Although the activation of the HPA axis during sexual maturation of Pacific salmon is similar to the axis activation during stress, the high levels of cortisol in salmon could be genetically programmed and not related to exposure to stressors (Dickhoff, 1989). Nevertheless, very high plasma corticosteroid levels in migrating salmon are similar to those occurring during periods of chronic stress (Hane et al., 1966; Fagerlund, 1967).
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THE EFFECTS OF STRESS AND GLUCOCORTICOIDS ON MEMORY |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Since we are concerned with the adaptive olfactory enhancement by cortisol in salmon, it is necessary to discuss the possible influence of cortisol on memory. It has been shown that chronic stress can impair both learning and memory (Luine et al., 1994
; Nishimura et al., 1999). Several studies have demonstrated that chronic stress reduces short-term (or "working") memory in laboratory rodents. For example, mice and rats exhibit a decrease in short-term food-storage memory after being repeatedly stressed (Luine et al., 1994). However, despite being implicated in short-term memory loss, stress also has been shown to enhance long-term (or "reference") memory (Cahill, 1997; Roozendaal and McGaugh, 1997). Chronic restraint stress enhances long-term spatial memory in rats performing eight-arm radial maze tests (Luine et al., 1996) and humans can experience enhanced memory for emotional events during periods of chronic stress (Bower and Sivers, 1998). |
CORTICOSTEROID RECEPTORS IN THE SALMON BRAIN |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Cortisol acts in the brain by binding to corticosteroid receptors (glucocorticoid receptors, GR) and initiating a biological response by interacting with DNA binding elements (Caamano et al., 1994
). Unoccupied corticosteroid receptors reside in the cytoplasm of the neuron, and, once occupied by hormone, they translocate into the neuronal nucleus (Caamano et al., 1994). Corticosteroid receptors have been identified in the teleost brain including the brains of several salmonid species. Receptors exhibiting a high binding affinity for glucocorticoids have been identified in the brain cytosol of juvenile chinook salmon (O. tshawytscha; Knoebl et al., 1996) as well as the hypothalamus (Allison and Omeljaniuk, 1998), pituitary, caudal telencephalon and anterior preoptic region in rainbow trout (O. mykiss; Teitsma et al., 1998, 1999). The distribution of GR in the kokanee salmon brain indicates that receptors are found in all major sites of HPA axis feedback (Carruth et al., 2000b). Cortisol can inhibit brain regions involved in the HPA axis that contain glucocorticoid receptors (GR), and also influence GR-containing neurons in regions not involved in HPA axis activation. |
POSSIBLE ADAPTIVE ROLE FOR STRESS IN SPAWNING PACIFIC SALMON |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Although the actions of cortisol on the hippocampus are usually considered to be deleterious (McEwen et al., 1986
; Jacobson and Sapolsky, 1991), this hormone could play an adaptive role in some organisms that require enhancement or recall of an imprinted critical memory. The olfactory pathways in the brain are intimately integrated with the hippocampus (Eichenbaum and Otto, 1992), and olfactory memory is important in many organisms (Math, 1993; Mouly et al., 1993). For example, memory of the "HSOB" is vitally important for the reproductive success of Pacific salmon. Cortisol, besides possibly causing the physical degeneration leading to death after spawning (see Dickhoff, 1989), also could have an adaptive influence in migrating salmon by enhancing their ability to recall the imprinted memory of the chemical composition of their home-stream water. In doing so, cortisol could act on olfactory receptors, olfactory sensory projections to the brain, and/or brain regions controlling olfactory memory storage or recall. |
GLUCOCORTICOID RECEPTORS IN KOKANEE SALMON OLFACTORY/MEMORY BRAIN REGIONS |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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The first step in determining what role cortisol might play in "HSOB" recall is to establish where the receptors that bind cortisol (glucocorticoid receptors, GR) are located in the kokanee salmon brain. Glucocorticoid receptor-like immunoreactive (GRir) neurons, identified via immunohistochemistry with an antibody to human GR (see Carruth et al., 2000b
for methods), are found in numerous kokanee brain regions including those involved with processing olfactory and/or memory information (Carruth et al., 2000b). In teleostean fishes, olfactory information is received by or projected to several brain regions such as the internal cell layer of the olfactory bulb (ICL; the primary olfactory center), as well as structures receiving secondary olfactory projections such as the ventral-lateral and lateral parts of the dorsal telencephalon (homologue of the mammalian hippocampus; Northcutt and Bradford, 1980; Northcutt and Davis, 1983), ventral area of the telencephalon (homologue of the mammalian amygdala; Northcutt and Bradford, 1980; Northcutt and Davis, 1983), and parvocellular neurons of the preoptic area (POA; Bass, 1981; Nieuwenhuys, 1982; Sas et al., 1993; Matz, 1995). The POA is involved in spawning behavior in fish (Nieuwenhuys, 1982; Satou et al., 1984; Shiga et al., 1985), and kokanee salmon utilize pheromones in their spawning interactions (Liley et al., 1993). Tertiary olfactory structures include the inferior lobe of the hypothalamus (IHL) and the glomerulosus complex of the thalamus which both receive olfactory information from the lateral telencephalon (Nieuwenhuys, 1982).
Kokanee salmon possess GRir in all of the olfactory and/or memory brain regions listed above (See Fig. 4), some of which also are involved in HPA axis feedback, such as the "hippocampus" and nuclei in the hypothalamus. Other non-olfactory regions with high GRir density are involved with negative feedback of cortisol on the HPA axis (Carruth et al., 2000b; Lederis et al., 1994) including the locus ceruleus, Raphe nucleus and nucleus of the solitary tract (Carruth et al., 2000b; see Figs. 4 and 5). The optic tectum and mesencephalic tegmentum have no known role in HPA axis function or olfaction and both also exhibited high GRir density (Carruth et al., 2000b; see Figs. 4 and 5).
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The brains from spawning kokanee also have significantly more GRir neurons (see Fig. 4), perhaps from upregulation, than do the brains of sexually immature kokanee salmon in all of the olfactory/memory related areas except one. Significant increases were observed in the ICL, "hippocampus," glomerulosus complex, parvocellular neurons in the POA, and the IHL, with only the "amygdala" showing no difference between the two sexual stages (Carruth et al., 2000b
). All of these brain regions have some involvement in olfaction (Nieuwenhuys, 1982) and could play a role in salmon homing and migration to natal spawning grounds.
There are also differences in intraneuronal location of GRir in olfactory regions, with staining being predominantly cytoplasmic in sexually immature fish but nuclear in spawning fish (See Table 1). Only two olfactory and/or memory brain regions, the ICL and parvocellular nucleus of the POA, do not contain significantly more nuclear stained GRir in spawning fish, both of which are continuously used for olfactory functions in all life history stages. These results are consistent with a role for cortisol in olfactory-mediated homing in kokanee salmon. Translocation of olfactory GRir neurons during kokanee migration and sexual maturation corresponds with the greatly elevated plasma cortisol levels present in kokanee at this stage of their life cycle (Carruth et al., 2000a; see Fig. 2). In addition, salmon GRir translocation, from cytoplasm into the nucleus, fits the classic theory described for mammalian GR, and could indicate brain regions of increased cortisol stimulation (van Eekelen et al., 1987). Therefore, the translocation of GR, which in mammals can be initiated by the binding of cortisol to GR (Caamano et al., 1994), could indicate the action of cortisol specifically on salmon olfactory structures.
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CORTISOL IN SEXUALLY IMMATURE FISH |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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The differences in GRir number and intracellular location between the two sexual stages (spawning and sexually immature) might be related to two factors. Firstly, the spawning fish have been exposed to higher levels of cortisol than the sexually immature fish and secondly, they were sexual mature and had experienced an activation of their hypothalamic-pituitary-gonadal axis. Sexual maturation has been demonstrated to modify the responsiveness of the HPA axis to stress in rainbow trout (O. mykiss), perhaps by altering the "set point" for cortisol negative feedback (Pottinger et al., 1995
). Additionally, androgen receptors (AR) have been demonstrated to interact with GR mRNA, in the hippocampus of rats (Kerr et al., 1996). Estrogen receptors (ER) are also located in mammalian brain regions, such as the hippocampus, containing GR (Bettini et al., 1992) and they may influence GR at the cellular level.
Sexually immature fish treated with an acute cortisol injection (either an intermediate or high dose) designed to raise plasma cortisol levels to within the range experienced by sexually mature, migrating Pacific salmon yielded mixed results (Carruth, 1998; see Fig. 6 and Table 2). A predicted difference in GRir neuronal number in some olfactory and/or memory brain regions, notably the "amygdala," the glomerulosus complex of the thalamus, and the IHL, failed to occur. Treating sexually immature fish with cortisol does not induce an up-regulation of GR to those levels observed in spawning fish in all olfactory-related brain regions (Carruth, 1998; see Fig. 6). The lack of complete GR up-regulation in these fish after cortisol treatment may be related to the sexual immaturity of the fish, as well as the duration of cortisol priming (Carruth, 1998). Acute cortisol treatment had the greatest effect on the location of GR within the neuron. In the ICL, the high cortisol-dose fish have almost 100% nuclear-stained neurons and cortisol-treated fish had significantly more nuclear-stained GRir neuronal cell bodies in the "hippocampus" than did non-cortisol primed fish.
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The cortisol treatment did not influence GRir number or percent nuclear staining in non-olfactory related brain regions. Two non-sensory control regions were examined, the optic tectum and the mesencephalic tegmentum, and showed no influence on GRir, in either neuronal number or intracellular translocation, after cortisol treatment (Carruth, 1998
). This supports a possible role for cortisol in the synthesis and translocation of GR in brain regions utilized for home-stream migration in Pacific salmon. |
CONCLUDING REMARKS AND FUTURE DIRECTIONS |
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SYNOPSISINTRODUCTIONHOMING IN PACIFIC SALMONPHYSIOLOGICAL AND HISTOLOGICAL...ACTIVATION OF THE HYPOTHALAMIC...THE EFFECTS OF STRESS...CORTICOSTEROID RECEPTORS IN THE...POSSIBLE ADAPTIVE ROLE FOR...GLUCOCORTICOID RECEPTORS IN...CORTISOL IN SEXUALLY IMMATURE...CONCLUDING REMARKS AND FUTURE...References |
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Cortisol is acting differentially on kokanee salmon brain regions that are involved with olfaction and/or memory when compared to regions related to HPA axis feedback. Spawning fish have more GRir in olfactory/memory brain regions as well as more GR translocated into neuronal nuclei. Additionally, priming sexually immature kokanee salmon with cortisol does not completely mimic the cortisol response observed in spawning fish. Potentially, GR sensitivity may be related to a variety of factors that include sexual maturity, age, or life history stage.
Our future research directions include investigating the influence of exogenous cortisol on electrophysiological activity of olfactory structures, as well as GR translocation in olfactory regions, of the kokanee salmon brain. The GR antagonist mifepristone (RU-38486) will be used to investigate the role of cortisol in olfactory migration in kokanee salmon. Finally, the possible stimulation of GR mRNA by sex steroids and receptor protein expression is worthy of investigation.
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ACKNOWLEDGMENTS |
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This study received generous support from the Colorado Division of Wildlife, and especially from J. Bennett, R. Kolecky and Dr. J. Woodling. T. Maldonado and G. Rosen offered valuable assistance with the collection of tissue and laboratory techniques as well as insightful discussions regarding the topic of this paper. Finally, we would like to thank J. Carr and C. Summers for organizing this symposium and for inviting LLC to participate. This research was supported by a NSF grant (IBN-9701027) to R. E. Jones and L. L. Carruth, and by a NSF grant (IBN-9603622) to R. E. Jones and D. O. Norris.
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FOOTNOTES |
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1 From the Symposium Stress—Is It More Than a Disease? A Comparative Look at Stress and Adaptation presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 Present address: Department of Biology, P.O. Box 4010, Georgia State University, Atlanta, Georgia 30302-4010; E-mail: lcarruth{at}gsu.edu
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