© 2002 by The Society for Integrative and Comparative Biology
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Stress, Neuropeptides, and Feeding Behavior: A Comparative Perspective1
1 Department of Biological Sciences, Texas Tech University, Box 4-3131, Lubbock, Texas 79409
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SYNOPSIS |
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Stress inhibits feeding behavior in all vertebrates. Data from mammals suggest an important role for hypothalamic neuropeptides, in particular the melanocortins and corticotropin-releasing hormone (CRH)-like peptides, in mediating stress-induced inhibition of feeding. The effects of CRH on food intake are evolutionarily ancient, as this peptide inhibits feeding in fishes, birds, and mammals. The effects of melanocortins on food intake have not been as extensively studied, but available evidence suggests that the anorexic role of neuronal melanocortins has been conserved. Although there is evidence that CRH and the melanocortins influence hypothalamic circuitry controlling food intake, these peptides may have a more primitive role in modulating visuomotor pathways involved in the recognition and acquisition of food. Stress rapidly reduces visually guided prey-catching behavior in toads, an effect that can be mimicked by administration of CRH, while corticosterone and isoproterenol are without effect. Melanocortins also reduce prey-oriented turning movements and, in addition, facilitate the acquisition of habituation to a moving prey item. The effects of these neuropeptides are rapid, occurring within 30 min after administration. Thus, changes in neuroendocrine status during stress may dramatically influence the efficacy with which visual stimuli release feeding behavior. By modulating visuomotor processing these neuropeptides may help animals make appropriate behavioral decisions during stress.
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INTRODUCTION |
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Most of us are reminded on a routine basis that stress affects appetite and food intake. The effects of stress on feeding are complex and depend upon a multitude of factors, not the least of which are the type, intensity, and duration of the stressor. Nonetheless, in every organism in which it has been studied, severe psychological or physical stress reduces appetite and food intake. To date, most research into this phenomenon has focused on the deleterious effects of stress on appetite in mammals, with an emphasis on understanding the physiological basis of stress-related eating disorders such as anorexia nervosa. Often overlooked in this approach is the fact that the neuronal and endocrine mechanisms involved in human eating disorders are evolutionarily ancient and have been conserved as part of a process for rapidly redirecting behavior in response to a threat. In the acute phase of this response, behaviors that are necessary for dealing with an imminent threat (avoidance, escape) emerge whereas feeding behavior is temporarily suspended. Examples of this behavioral hierarchy appear in every vertebrate group (Gilliam and Fraser, 1987
; Abrahams and Sutterlin, 1999; Carrascal and Polo, 1999; Lilliendahl, 2000; Whitham and Mathis, 2000; Ziemba et al., 2000).
How do animals redirect behavior in response to a threat? The antipredator behavior of anuran amphibians serves as an example. For a toad, the decision to search for food in the presence of a predator (snake) increases the likelihood that it will be captured and eaten (Heinen, 1994). In contrast, if a toad stops moving and assumes a cryptic posture, it is less likely to be contacted by a snake and subsequently eaten (Heinen, 1994). At the heart of this behavioral decision making process are elementary visuomotor pathways that have evolved to rapidly redirect behavior in response to a threat. These pathways are remarkably sensitive to the homeostatic and endocrine status of the organism, in particular to hormones released during stress.
The goal of this short review is twofold. The first goal is to briefly review the effects of stress and stress hormones on feeding in vertebrates. Although a number of hormones have been implicated in stress-induced feeding changes, this review will focus on the role of neuropeptides. The second goal is to examine the effects of stress and stress hormones on anuran prey-catching as a means of illustrating the role of neuropeptides in redirecting behavior during stress.
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A COMPARATIVE LOOK AT STRESS AND FEEDING BEHAVIOR |
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A large volume of research indicates that stress affects feeding in mammals in a manner that depends upon the duration and intensity of the stressor. Particularly intense painful (Antelman and Szechtman, 1975
; Holland et al., 1977) or psychologically threatening (Shimizu et al., 1989) stressors inhibit feeding (Table 1). In particular, physical restraint in rodents has been used as a model for anorexia nervosa (Rybkin et al., 1997), mainly because of its psychological nature. In contrast, so-called mild stressors, such as a gentle tail-pinch in rats, can cause spontaneous feeding (Morley et al., 1983). Endogenous opioids seem to play a critical role in stress-induced eating (Morley et al., 1983).
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Stress-induced alterations in feeding are not restricted to mammals. Table 1 shows that a wide variety of stressors affect feeding behavior in fishes, birds and mammals, the groups that have been best studied. This table is not meant to be exhaustive but rather to highlight the diversity and non-specific nature of the stressors that affect feeding. This is an important point to keep in mind when considering the complexity of the hypothalamic neuropeptidergic interconnections that govern stress-induced changes in feeding.
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STRESS-RELATED NEUROPEPTIDES AND FEEDING BEHAVIOR |
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SYNOPSISINTRODUCTIONA COMPARATIVE LOOK AT... STRESS-RELATED NEUROPEPTIDES AND... STRESS AND FEEDING: ECOLOGICAL...HOW DO NEUROPEPTIDES INFLUENCE...THE ADAPTIVE SIGNIFICANCE OF...CONCLUSIONSReferences |
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Several lines of evidence implicate hypothalamic neuropeptides in the regulation of feeding. First, central administration of hypothalamic neuropeptides affects food intake and weight gain in mammalian and nonmammalian vertebrates (see Inui, 1999
; Ahima et al., 2000; Lin et al., 2000 for recent reviews). Secondly, lesions of the hypothalamus have well-described effects on feeding behavior in humans (Celesia et al., 1981) and lab mammals (Kalra et al., 1999). Third, spontaneous genetic mutations or targeted gene deletions that impair hypothalamic neuropeptide function have dramatic effects on feeding. Research into the mechanism of leptin action has revealed that hypothalamic neuropeptides involved in coordinating the neuroendocrine stress response, particularly the melanocortins and corticotropin-releasing hormone (CRH), play a pivotal role in the normal maintenance of body weight and energy metabolism. At the core of these regulatory mechanisms lay complex interconnections between discrete hypothalamic nuclei including the arcuate nucleus, the lateral hypothalamic area (LHA), and the paraventricular nucleus (PVN). Although several hypothalamic peptides have been implicated in the regulation of feeding, I will focus on two peptide families that have been linked to stress-induced alterations in feeding.
Arcuate melanocortin neurons
Subsets of cells in the arcuate nucleus produce the pro-hormone proopiomelanocortin (POMC). Post-translational cleavage of POMC results in a number of biologically active peptides including ß-endorphin (ßE) and the melanocortin peptides, corticotropin (ACTH) and alpha-melanocyte-stimulating hormone (
MSH). Evidence supporting a physiological role of melanocortins in feeding behavior came initially from interest in the biological basis for coat color in agouti mice. These mice ubiquitously over-express the agouti protein, an endogenous melanocortin receptor antagonist (Lu et al., 1994). As a result, they develop a yellow coat. However, agouti mice also develop a form of late-onset obesity similar to that occurring in mice deficient in the melanocortin MC-4 receptor (Huszar et al., 1997). MC-4 receptor antagonists block leptin effects on weight gain (Seeley et al., 1997) while direct intracerebroventricular (i.c.v) administration of an MC-4 agonist inhibits feeding in a wide variety of hyperphagic models (Fan et al., 1997). Leptin increases POMC expression in arcuate neurons while leptin deficient mice express 50% less POMC in the arcuate nucleus than wild-type mice (Schwartz et al., 1997). A similar reduction in POMC expression is observed in fasted mice (Schwartz et al., 1997). These findings, with evidence that leptin receptors are expressed within arcuate POMC neurons (Cheung et al., 1997; Håkansson et al., 1998), point to a critical role for melanocortins in regulating feeding behavior. Melanocortins inhibit feeding in amphibians and birds (Table 2), suggesting an evolutionarily ancient role as anorexigenic neuropeptides. Although disruption of ßE signaling does not result in the dramatic effects on weight gain observed with targeted disruption of melanocortin receptors (Huszar et al., 1997), direct i.c.v administration of this peptide increases feeding (McKay et al., 1981; Table 2).
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Paraventricular nucleus and CRH-like peptides
The PVN contains hypophysiotropic CRH neurons that also play a role in the CNS control of feeding. CRH potently inhibits feeding in every vertebrate group so far examined (Table 2). A second CRH-like peptide, urocortin, produced by neurons in the Edinger-Westphal nucleus (Vaughan et al., 1995
), may also be involved in feeding in mammals; urocortin is a more potent inhibitor of feeding than CRH when administered i.c.v. (Spina et al., 1996). The receptor(s) mediating these effects appear to have been evolutionarily conserved, as fish urotensin I inhibits feeding in both fish (Bernier and Peter, 2001a) and mammals (Negri et al., 1995). The role of CRH-like peptides and their receptors in feeding is complex and beyond the scope of this paper; the reader is referred to recent discussions on the topic (Heinrichs and Richard, 1999; Bradbury et al., 2000; Cone, 2000). Nonetheless, the physiological importance of the PVN is clear, especially given the recent evidence that the PVN may be the principal site of convergent orexic and anorexic signals from the arcuate and LHA, thereby functioning as sort of an "adipostat" (Cowley et al., 1999).
Hypothalamic neuropeptides mediate stress-induced changes in feeding behavior
Given the involvement of melanocortins and CRH in mediating leptin action, it is not surprising to see that some of these same neuropeptides are involved in stress-induced affects on feeding. Restraint-stress induced anorexia in rats is partially-reduced after administration of the CRH-receptor antagonist -helical CRH (9–41) (Krahn et al., 1986) and is completely inhibited by immunoneutralization of CRH (Shibasaki et al., 1988). CRH is also involved in anorexia nervosa, as CSF CRH is elevated in patients with this disorder (Hotta et al., 1986). A role for melanocortins is suggested by evidence that administration of the MC4 antagonist HS014 reduces stress-induced anorexia (Vergoni et al., 1999a). The effects of CRH are not mediated by the melanocortins, as HS014 does not block CRH-induced anorexia (Vergoni et al., 1999b).
An interesting problem arises when one considers that ßE and MSH are produced from the same pro-hormone (POMC) but have opposite effects on feeding. Nonetheless, feeding-related changes in arcuate POMC expression generally support an anorexigenic role for these neurons. Neurotoxin-induced transient hyperphagia and weight gain are both associated with decreased POMC expression and levels of MSH in the PVN, effects that can be reversed with administration of the non-selective MC-3/MC-4 agonist MT-II (Dube et al., 2000). Obese Zucker rats have lower arcuate POMC gene expression and reduced MSH content in the PVN compared to lean Zucker controls (Kim et al., 2000). Interestingly, ßE content in the PVN is unchanged in obese Zucker rats, suggesting differential secretion and/or metabolism of POMC end-products in the PVN (Kim et al., 2000).
Stress and prey-catching in anuran amphibians
Although the neuropeptidergic control of feeding has been studied in nonmammals, particularly in fishes (Lin et al., 2000), little is known about the role of neuropeptides in stress-induced inhibition of feeding in nonmammals (Bernier and Peter, 2001b). We have examined the role of stress-related neuropeptides in a simple model of visually-guided feeding in toads. Toads generally feed on small insects such as worms, ants, crickets, and beetles. Movement and configurational aspects of these prey-stimuli are pre-programmed in the toad's CNS. Presenting a toad with a cardboard rectangle of the appropriate configuration (long axis parallel to direction of movement = worm) triggers the same series of ballistic movements (orienting 
approaching snapping) that a toad would perform in response to real prey. Exposure to a noxious stimulus (ether vapors) or crowding inhibit prey-catching (Carr et al., 2002). Adult toads respond to noxious stimuli by releasing corticosterone (Olsen et al., 1999), presumably due to CRH activation of the pituitary-adrenal axis, as in mammals. Administration of ovine CRH (oCRH), a form of the peptide that is weakly sequestered by CRH binding proteins (Valverde et al., 2001), causes a similar reduction in prey-catching behavior (Carr et al., 2002). Interestingly, toads treated with oCRH developed a marked pupillary dilation within 30 min (Zozzaro and Carr, 2002), an indication of sympathetic stimulation (Morris, 1976). This is not entirely unexpected, as CRH acts on CNS receptors to activate the sympathetic nervous system in mammals (Brown et al., 1982). The effects of CRH on prey-catching probably do not involve sympathetic stimulation, however, as administration of isoproterenol at a dose sufficient to cause maximal pupillary dilation does not affect responsiveness to a prey-item (Carr et al., 2002). The effects of oCRH are apparently not mediated by adrenocorticosteroid secretion, as administration of a dose of corticosterone that elevates blood levels of the steroid to those seen during stress (Carpenter and Carr, 1996; Olsen et al., 1999) has no effect on prey-catching behavior (Carr et al., 2002).
Several lines of evidence suggest that melanocortins may be involved in stress-induced reductions in prey catching. Early work by Horn et al. (1979) demonstrated that ACTH facilitated acquisition and delayed extinction of habituation to a prey-dummy. Work in our lab confirmed the work of Horn et al. (1979) and extended these findings by showing that MSH and ACTH 4–10 but not des-acetyl MSH or (Nle4, D-Phe7) -MSH facilitated acquisition (Carpenter and Carr, 1996). The effects of melanocortins on habituation to a prey-item are dose-dependent, are not mediated by adrenal corticosteroids, and are direction and stimulus specific, suggesting that they are not due to fatigue or some type of non-specific sedative effect (Carpenter and Carr, 1996; Olsen et al., 1999). The effects of MSH on acquisition may be mediated by CNS receptors, as radiolabeled MSH is detected in CSF within 30 min after dorsal lymph sac injection (Olsen et al., 1999).
The ability of melanocortins to influence habituation is intriguing, given the similarity between habituation and aversive (or threatening) stimulus effects (Ingle, 1983) and the fact that both habituation and response to a threat are driven by the pretectum (Ewert, 1980). Melanocortins affect stress-related behaviors in mammals, such as grooming (von Frijtag et al., 1998), a behavior characteristically elicited in response to a threatening stimulus. Immunoneutralization of central ACTH decreases novelty-induced grooming in rats (Dunn et al., 1979).
Two major lines of evidence suggest an endogenous role for neuronal melanocortins in regulating feeding behavior in toads. First, melanocortin neurons innervate areas involved in visuomotor processing (Rana ridibunda, Benyamina et al., 1986; Bufo cognatus, Kim and Carr, 1997; Xenopus laevis, Tuinhof et al., 1998; Spea multiplicata, Venkatesan and Carr, 2001). A second line of evidence is work in our lab showing that that brain MSH is altered during and after exposure to a noxious stimulus (Olsen et al., 1999) or confinement (Kim and Carr, 1997). In response to both types of stressors there is a marked decrease in telencephalic MSH content, suggesting increased release of the peptide by ascending melanocortin projections.
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STRESS AND FEEDING: ECOLOGICAL AND ETHOLOGICAL PERSPECTIVES |
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SYNOPSISINTRODUCTIONA COMPARATIVE LOOK AT...STRESS-RELATED NEUROPEPTIDES AND...STRESS AND FEEDING: ECOLOGICAL...HOW DO NEUROPEPTIDES INFLUENCE...THE ADAPTIVE SIGNIFICANCE OF...CONCLUSIONSReferences |
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What are the selective forces guiding the evolution of hypothalamic circuits for inhibiting feeding during stress? To answer this question it is necessary to understand the costs associated with feeding for animals living in their natural environment. An increasing body of literature supports the idea that animals weigh the benefits of feeding with a number of costs, one of the most important being risk of predation (Ziemba et al., 2000
). The long-term consequences of the tradeoff between foraging and predation risk have been best-studied in birds. In birds, maintenance of fat reserves is required to sustain energy metabolism during periods when the animal cannot eat. Most birds, however, maintain fat stores well below the physiological maximum, presumably because increased fat stores (and consequently increased body weight) increase the risk of predation (Witter and Cuthill, 1993). Simply stated, an obese bird can quickly become a dead bird if it is unable to escape a predator. Increasing body mass can hinder take-off and escape from a predator (reviewed in Lilliendahl, 2000). In addition, maintenance of increased body mass requires that the animal spend more time foraging, thereby exposing itself to potential predators. Birds reduce food intake and lose weight when exposed to real or simulated predators (Carrascal and Polo, 1999; Lilliendahl, 2000).
Predation risk can guide the evolution of neuronal pathways that allow the animal to rapidly redirect behavior in response to a threat, a phenomenon most clearly seen in animals with an elementary behavioral repertoire, such as frogs and toads. Toads respond to a predator such as a snake with a series of pre-programmed behaviors that include an immediate cessation of movement and a crouching posture. Large looming objects, sometimes even an otherwise optimal prey-stimulus (see above) oriented vertically (long axis perpendicular to movement direction = anti-worm), can elicit the same avoidance posture observed in response to a snake (Ewert, 1980). If predator and prey stimuli are presented simultaneously during the feeding season, avoidance/escape behavior overrides feeding (Ewert, 1997). A similar behavioral hierarchy exists in other vertebrates. Both wild-type and growth-enhanced transgenic Atlantic salmon reduce foraging in the presence of a predator (Abrahams and Sutterlin, 1999) while salamanders wait longer before attacking prey when presented with chemical cues from a natural predator (Whitham and Mathis, 2000). Tiger salamander larvae will reduce feeding to avoid being preyed upon by conspecific cannibalistic salamanders (Crowley and Hopper, 1994). Smaller non-cannibalistic salamanders respond to conspecific cannibals as a threat, and presumably forage less to decrease the likelihood of being detected and eaten by the larger cannibal forms (Ziemba et al., 2000). Captive greenfinches (Carduelis chloris) stop foraging and lose body mass in the presence of a perceived predator (Lilliendahl, 2000).
The neuroanatomical pathways underlying predator/prey decision making have been well studied in anurans. Anatomical, electrophysiological, and behavioral/lesion studies support a retinal tectum/pretectum medullary spinal cord pathway for responding to prey (Fig. 1A). At least seven types of tectal neurons that respond to various aspects of prey-configuration and project to medullary motor control areas have been identified (Ewert, 1997). Retino-recipient neurons in the caudal thalamus/pretectum drive predator avoidance behavior, in part via an inhibitory interaction with the tectum (Fig. 1B). So-called "predator-detector" neurons in the pretectum (class TH3 and TH4 according to Ewert, 1997) project to the ipsilateral tectum and inhibit tectal firing. Lesioning the pretectum eliminates avoidance behavior and prevents the habituation that normally occurs when a non-rewarding prey-stimulus is presented repeatedly over time. Over-driving the pretectal-tectal inhibitory pathway completely eliminates prey-catching, a phenomenon illustrated by lesioning the ventral striatum (Finkenstädt, 1987). This brain area indirectly modulates tectal bug-detector cells by tonically inhibiting the pretectum through fibers carried in the lateral forebrain bundle (Ewert et al., 1999; Fig. 1B). Lesioning the striatum "releases" pretectal-tectal inhibitory neurons, and the animals do not respond to prey (Finkenstädt, 1989; Patton and Grobstein, 1998).
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HOW DO NEUROPEPTIDES INFLUENCE WHAT THE TOAD'S EYE TELLS THE TOAD'S BRAIN? |
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SYNOPSISINTRODUCTIONA COMPARATIVE LOOK AT...STRESS-RELATED NEUROPEPTIDES AND...STRESS AND FEEDING: ECOLOGICAL...HOW DO NEUROPEPTIDES INFLUENCE...THE ADAPTIVE SIGNIFICANCE OF...CONCLUSIONSReferences |
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Recent anatomical studies support the concept that hypothalamic neuropeptides target sensory and motor circuits involved in simple decision making processes, such as predator/prey recognition. In amphibians and reptiles, melanocortins innervate basal forebrain structures involved in subcortical visuomotor processing, specifically the basal ganglia (Khachaturian et al., 1984
; Benyamina et al., 1986; Kim and Carr, 1997; Tuinhof et al., 1998; Venkatesan and Carr, 2001; Fig. 1C). In toads, the basal ganglia are innervated by POMC neurons (Kim and Carr, 1997; Venkatesan and Carr, 2001). The striatum (and to a lesser degree the nucleus accumbens) supply both direct and indirect innervation to the optic tectum (Wilczynski and Northcutt, 1983; Marin et al., 1997, 1998). By innervating the basal ganglia, melanocortin neurons may gain access to multiple modes of tectal regulation.
Both CRH- and sauvagine-immunoreactive neurons have been identified in the nucleus of the medial longitudinal fasciculus (nMLF) in the mesencephalic tegmentum of anurans. Neurons in the nMLF drive spinal motor and interneurons in fish (Bosch et al., 1995; Uematsu and Todo, 1997) and may participate in mediating tecto-spinal information flow during prey-orienting behaviors (Kostyk and Grobstein, 1987; Masino and Grobstein, 1989). Whether CRH- or sauvagine neurons in the nMLF participate in stress-induced inhibition of prey-catching remains to be seen, but deserves consideration given the well-documented effects of CRH on locomotor activity in fishes (Clements and Schreck, 2001), amphibians (Moore et al., 1984; Lowry et al., 1990) and mammals (Dunn and Berridge, 1990). In newts, CRH alters the discharge patterns of medullary neurons involved in locomotor behaviors (Lowry et al., 1996).
One could easily argue that stress-related neuropeptides affect feeding motivation simply by elevating blood glucose titers. Elevated blood glucose rapidly (within 15 min) shuts down feeding motivation in toads (Laming and Cairns, 1998). However, this is not a likely mechanism for melanocortin action as the effects of ACTH on habituation are stimulus and direction specific (Horn and Horn, 1982; Carpenter and Carr, 1996). CRH has a slight but rapid hyperglycemic effect in rats that is mediated via sympathetic stimulation (Brown et al., 1982). However, isoproterenol has no effect on prey-catching (Carr et al., 2002). Whether CRH effects blood glucose within the 30 min time frame in which we see affects remains to be seen.
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THE ADAPTIVE SIGNIFICANCE OF REDIRECTING BEHAVIOR DURING STRESS |
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Is stress-induced inhibition of feeding adaptive? Studies on the antipredator behavior of toads can provide insight into this question. According to Endler (1991)
, organisms evolve antipredator behaviors in concert with the major sensory mode(s) used by predators. Garter snakes are more likely to use visual over olfactory cues when hunting toads (Heinen, 1995). In turn, toads respond to a visual image of a snake by reducing their movement and crouching low to the ground, this latter behavior being identical to the avoidance behavior generated by electrical stimulation of the pretectum (Ewert, 1980). Unfed toads are more likely to remain active in the presence of a predator and subsequently more likely to be caught (Heinen, 1994). These studies suggest that the degree of satiety can directly impact a toads survival in the presence of a predator, which raises the speculative (and presently untested) question: Are melanocortins and CRH satiety and/or antipredator peptides? It is not unreasonable to imagine that the satiety effects of these peptides are just one component of a suite of defensive responses engaged in a threatening situation. |
CONCLUSIONS |
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Exposure to severe physical or psychologically threatening stressors inhibits feeding in all vertebrates. In mammals, hypothalamic neuropeptides such as CRH and the melanocortins play a critical role in stress-induced changes in feeding. Although there have been remarkable advances in identifying intra-hypothalamic pathways involved in stress-induced feeding disorders (Cowley et al., 1999
; Bell et al., 2000), precisely how this information is parceled out of the hypothalamus to brain areas involved in feeding motivation is poorly understood. Research on anurans suggests that stress-related neuropeptides interact with elementary visuomotor pathways to inhibit visually-guided feeding behavior. These pathways are directly affected by motivational state (Laming and Cairns, 1998) and ensure that appropriate motor patterns are rapidly engaged in response to changes in the animal's visual environment, such as the presence of a predator. Pretectal-tectal inhibitory pathways ensure a rapid suspension of feeding and emergence of appropriate avoidance behaviors. Pretectal-tectal inhibitory neurons are influenced, in turn, by inhibitory neurons in the striatum, a target for melanocortin innervation in nonmammalian vertebrates. Whether melanocortins and CRH act to reduce feeding motivation or to engage antipredator behaviors is a major question for future research. At least some of the effects of CRH on feeding may be independent of stress-induced escape and fear-related behaviors, as peripheral administration of urocortin reduces the rate of gastric emptying in lab rodents (Asakawa et al., 1999; Wang et al., 2001). Although the adaptive significance of reducing feeding behavior in response to a predator has been demonstrated experimentally, a major question that remains is why do animals respond in virtually the same way to such a wide variety of non-specific threats (Table 1)? The answer probably lies in understanding how afferent sensory information is directed to hypothalamic neuropeptidergic areas involved in feeding. The interactions between hypothalamic neuropeptides and visuomotor processing in the toad provides a simple model for dissecting out how neuropeptides influence behavioral decision making during stress.
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ACKNOWLEDGMENTS |
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The studies reported here were supported in part by funds from the Texas Tech University Research Enhancement Fund, a Howard Hughes Medical Institute grant through the Undergraduate Biological Sciences Education Program to TTU, and the NIH (MH53065). The symposium was made possible by funding from the NIMH (R13 MH62670), NSF (IBN 0100532), the Center for Biomedical Research Excellence (CoBRE, CHS) at the University of South Dakota on Neural Mechanisms of Adaptive Behavior, South Dakota EPSCoR, and the USD Office of Research.
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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 E-mail: jacarr{at}ttacs.ttu.edu
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