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Brain, Hormone and Behavior Interactions in Avian Reproduction: Status and Prospectus

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Brain, Hormone and Behavior Interactions in Avian Reproduction: Status and Prospectus The Condor91:966-978 Q The CooperOrnithological Society 1989 BRAIN, HORMONE AND BEHAVIOR INTERACTIONS IN AVIAN REPRODUCTION: STATUS AND PROSPECTUS RAE SILVER Department of Psychology,Barnard Collegeof Columbia University,3009 Broadway, New York, NY 10027 GREGORY F. BALL Department of PsychologyBoston College,Chestnut Hill, MA 02167 Abstract. The centralnervous system transduces behaviorally significant environmental informationnecessary for successfulreproduction. Convergent lines of researchsuggest that a numberof questionsregarding the natureof speciesdifferences, and how thesedifferences havebeen implemented over evolutionary time, canbe approachedthrough the clarification of underlyingbrain mechanisms.The last 15 yearshave yieldeda host of techniquesfor studyingthe integrationby the nervoussystem of sensory,neural, and endocrinefactors mediatingspecies typical reproductivebehaviors. In this paper,we review major issues relevantto our presentunderstanding of environmental-brain-endocrinebehavior relation- shipsin avian breedingsystems, and indicatethe techniques that are now available to explore neuralmechanisms. Specifically, we discussrecent evidence on thelocalization of encephalic photoreceptors,the biologicalclock and its putativerole in timing breedingcycles, pepti- dergic(gonadotropic hormone releasing hormone, GnRH, and vasoactiveintestinal poly- peptide,VIP) influenceson the pituitary-gonadalaxis, and the neurochemicalconsequences of hormoneaction in the avian brain. INTRODUCTION Lehrman 196 1, Mm-ton and Westwood 1977, It has been known for centuries that stimuli from Wingfield and Farner 1980, Follett 1984). the environment profoundly influence reproduc- In the decadessince Harris ’s discovery,we have tive physiology and behavior. Though many learned a great deal about environmental factors studies have documented the link between en- regulating reproduction. A complete understand- vironmental changesand endocrine physiology, ing of the ultimate causesof diverse reproductive the mechanisms underlying these changeswere strategies and of the evolution of associated not understood until well into the 20th century. mechanisms still eludes us. The classicissues of A major advance in our understandingof brain- why and when animals do as they do, however, hormone-behavior-environment interactions in terms of underlying hormonal mechanisms rested on the establishment of a route whereby have been successfullyaddressed in both labo- the CNS could mediate the complex interaction ratory and field studieson behavioral, endocrine, between endocrine functioning and behavioral and neural mechanisms of reproduction (Cheng and environmental signals. In 1955, Geoffrey 1979; Silver 1978; Silver and Cooper 1983; Harris demonstrated conclusively the existence Wingfield and Famer 1980; Silverin 1983, 1988; of a humoral link between the brain and the pi- Wingfield 1983; Wingfield et al. 1987). tuitary gland via the pituitary portal system.This Prominent featuresof the basic anatomical or- vascular connection is the route whereby signals ganization of the HPG are shared by all major from the brain reach the pituitary gland and vertebrate groups.Secretory neurons in the brain thereby have accessto the general blood supply synthesize a hormone-gonadotropic hormone of the body. We now know that such responses releasing hormone (GnRH)-which communi- are mediated by the hypothalamo-hypophyseal- cates with the hypophysis via a vascular con- gonadal (HPG) axis. In particular, it now appears nection-the pituitary portal system. Stimula- that these environmentally influenced reproduc- tory glycoprotein hormones-gonadotropins- tive phenomena are regulated by changesin hor- are secretedby the pituitary gland, which in turn mones circulating in the blood (Marshall 1959, initiate hormone secretion by the gonads. Go- nadal steroidsmay stimulate or inhibit the func- tional status of the neural and/or pituitary com- LReceived 25 May 1989. Final acceptance26 July ponents. 1989. There is a distinct pattern of changes in [9661 REVIEW 967 steroid and pituitary hormones correlated with mechanisms underlying speciesdifferences and behavioral and physiological events of the re- individual differencesin reproductive cyclesand productive cycle (Silver 1978, Cheng 1979, Far- reproductive behavior in birds may well be elu- ner and Follett 1979, Wingfield and Farner 1980, cidated by examining the target sites for hor- Follett 1984, Wingfield et al. 1987). The tem- mones in the brain. poral pattern ofhormone secretioninfluences the progression from one stage of the reproductive NEURAL PROCESSES IN AVIAN cycle to the next. The onset ofbreeding is marked REPRODUCTION by an increase in the secretion of pituitary go- At the level of the brain one can study the in- nadotropins (luteinizing hormone-LH, and fol- tegration of external environmental stimuli and licle-stimulating hormone-FSH) and gonadal internal bodily signals,and how these signals in- steroids,androgens (such as testosteroneand 50(- fluence the neural substrate.A cascadeof events dihydrotestosterone)in males and estrogens(such are involved in this process:(1) specialized re- as 17p-estradiol) in females. These hormones re- ceptors for the external signals transduce the main above nonbreeding baseline levels physical stimuli into neural events, (2) pathways throughout the breeding season. In all species from various receptorsreach target areas in the there is a rise in prolactin secretion associated brain, including the biological clock and neurons with incubation and/or brooding (Goldsmith elaborating releasing hormones in the preoptic 1983). area and hypothalamus,(3) neuromodulatory and Even though these hormone-behavior rela- enzymatic factors regulate the releasing hor- tionships have been established,the causeof the mones, and (4) peripheral steroid hormones hormone changesand consequencesof these en- themselves act back on the brain to alter its re- docrine changes remain to be fully explained. sponsiveness.To illustrate both the current sta- Also, knowledgeof endocrine changesalone leave tus of our understanding, and the methods used several other issues unresolved. Thus, surpris- to address these issues, we will discuss each of ingly, significant differences in social behavior these events in turn. among speciesare associatedwith relatively small differences in hormone secretion. For example, RECEPTORS FOR ENVIRONMENTAL STIMULI two specieswith natural history patternsthat vary Temperate zone birds limit their reproductive from the typical avian pattern, the brood-para- activity to a particular time of the year. This sitic Brown-headedCowbird (Molothrusater) and involves responsesto both photoperiodic infor- the polyandrous Spotted Sandpiper (Actitisma- mation and to supplementary cues such as be- cularia),have endocrine profiles of gonadotro- havioral interactions, the availability of nest sites, pins, sex steroids, and prolactin that are similar nest material, and food (Wingfield 1983, Famer in many ways to those previously identified for 1986). If we could identify the sensoryreceptors monogamous biparental species. The Spotted that transduce environmental cues this would Sandpipers exhibit reversed behavioral sex roles represent an important first step in understand- that are not based on a total reversal of the nor- ing how changesin hormone secretion are pro- ma1 male to female ratio of androgens to estro- duced by the brain. This in turn would set the gens (Fivizzani and Oring 1986). Brown-headed stagefor understanding speciesdifferences in re- Cowbirds which remain sexually active through- sponsivenessto environmental factors, and the out the breeding season show hormone profiles way in which mechanisms constrain the evolu- quite similar to parental species in the sexual tionary lability of reproductive systemsin birds. phase of the annual cycle (see Dufty and Wing- Of the relevant environmental stimuli, photic field 1986 for review). In a similar vein, indi- cues have been the most intensively studied. vidual differences in behavior within a given Photoperiodic cues provided by daylength de- population are generally not reflected by differ- termine whether the reproductive system is in ences in hormone secretion in mammals (Da- an active or inactive state, while supplementary massa et al. 1977, Harding and Feder 1976) cues accelerateor retard this process(Wingfield though at least one mammalian study has found 1983, Follett 1984, Famer 1986). In birds, pho- such individual differencesto be correlated with toperiodic information is detectedby an extraret- brain differences in hormone receptor levels inal encephalic photoreceptor while the supple- (Clark et al. 1985). These issues related to the mentary information is processedby the ears and 968 RAE SILVER ANDGREGORY F. BALL eyes. Benoit (1935) demonstrated that blinded in the septal and tuberal hypothalamic regions Mallard drakes (Anus platyrhynchos L.) contin- of the dove and duck brain (see Fig. 1). These ued to recrudescetheir testes in responseto ar- opsin positive perikarya also express another tificial photostimulation. The existence of en- peptide, namely vasoactive intestinal polypep- cephalic photoreceptors has been well tide (VIP). Thus, for the first time, we have a documented in a variety of avian species(Oliver potential anatomical marker for this brain pho- and BaylC 1980). One of the most recent analyses toreceptor. It should be noted that although this of the encephalic photoreceptor established an result is highly suggestive,it
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