Neural and hormonal mechanisms of reproductive-related arousal in fishes

15 Pages·2011·1.05 MB·English

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HormonesandBehavior59(2011)616–629
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Hormones and Behavior
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Review
Neural and hormonal mechanisms of reproductive-related arousal in fishes
Paul M. Forlanoa,⁎, Andrew H. Bassb
aDepartmentofBiologyandAquaticResearchandEnvironmentalAssessmentCenter,BrooklynCollegeofTheCityUniversityofNewYork,2900BedfordAve,Brooklyn,NY11210,USA
bDepartmentofNeurobiologyandBehavior,CornellUniversity,Ithaca,NY14853,USA
a r t i c l e i n f o a b s t r a c t
Articlehistory: Themajorclassesofchemicalsandbrainpathwaysinvolvedinsexualarousalinmammalsarewellstudied
Received28September2010 andarethoughttobeofanancient,evolutionarilyconservedorigin.Herewediscusswhatisknownofthese
Accepted2October2010 neurochemicalsandbraincircuitsinfishes,theoldestandmostspecies-richgroupofvertebratesfromwhich
Availableonline13October2010
tetrapods arose over 350million years ago. Highlighted are case studies in vocal species where well-
delineatedsensoryandmotorpathwaysunderlyingreproductive-relatedbehaviorsillustratethediversity
Keywords:
andevolutionofbrainmechanismsdrivingsexualmotivationbetween(andwithin)sexes.Alsodiscussedare
Teleost
evolutionaryinsightsfromtheneurobiologyandreproductivebehaviorofelasmobranchfishes,themost
Elasmobranch
POA ancientlineageofjawedvertebrates,whichareremarkablysimilarintheirreproductivebiologytoterrestrial
AVT mammals.
GnRH ©2010ElsevierInc.Allrightsreserved.
Monoamines
Steroidreceptors
Vocal-acoustic
Neuroethology
Contents
Introduction:Evolutionarilyconservedneurochemicalsandpathwaysofsexualarousal. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 616
Whatisknownoftheneuralcircuitryof“sexualarousal”infishes?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 617
Connectivity,neurochemistryandfunctionofthePOA/anteriorhypothalamus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 617
GnRHintheterminalnerveganglion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 618
Olfactorypathwaysandsexualbehavior. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619
Neurochemicalarousalpathwaysinthe“paracore”. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 620
Steroidhormonereceptorsincircuitsinvolvedinreproductivebehavior. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
Brainarousalandreproductivebehaviorinvocalfishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 623
Neuralsubstratesforsexualarousalandreproductivebehaviorinelasmobranchfishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 623
Concludingcomments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 625
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 625
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 625
Introduction: Evolutionarily conserved neurochemicals and originating from what Nieuwenhuys et al. (1988) define as the
pathwaysofsexualarousal neurochemically rich “core” and “paracore” that together form a
neuroendocrine“axis”inthebrain.Coreregions,likethepreopticarea
Mongetal.(2003)commentthat“higharousalisreflectedbyhigh (POA), lie adjacent to the brain's ventricular spaces and contain
sensory responsiveness, high motor activity, and high emotional neuronalpopulationsthatsynthesizeawiderangeofneuropeptides,
reactivity.”Ultimately,changesinlevelsofarousalofanyonesensory concentrateandrogensandestrogens,andarebroadlyimplicatedin
or motor system depend on some form of modulatory input thecontrolofhomeostaticandsocialbehaviors.Alaterallypositioned
“paracore”regionatbrainstemlevelsisespeciallyrichinmonoamines
(serotonin and catecholamines) and interconnected with the core
⁎ Correspondingauthor.Fax:[phone].
region.Thesepeptidergic-containingnucleiandtheirfibertractscan
E-mailaddresses:[email protected](P.M.Forlano),[email protected]
(A.H.Bass). bedesignatedasacaudallyextendedlimbicsystemthatincludesthe
0018-506X/$–seefrontmatter©2010ElsevierInc.Allrightsreserved.
doi:10.1016/j.yhbeh.2010.10.006
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P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629 617
midbrain periaqueductal gray, the nucleus of the solitary tract and (Fig.2).ThePOA'seffectonhomeostaticfunctionisenhancedbyway
areapostremainthecaudalmedulla,andthecentralgrayofthespinal ofcentralvisceromotorinnervationofautonomicgangliathatproject
cord (Nieuwenhuys et al., 1988). The core–paracore regions also toeitherglands(includingtheadrenalmedulla,amodifiedautonomic
includetheessentialnodesofaproposed“socialbehaviornetwork” ganglion)orthevisceralsmoothmuscleofmultipleorgansystems.
forvertebrates(Goodson,2005;Newman,1999).Insum,thishighly The POA's pervasive influence on neuroendocrine function is
conservedareaofthevertebratebrainsuggestsitskeyroleinsurvival achieved,inpart,viaitscontroloverthereleaseofseveralpeptides
bymodulatingbrainarousaltoaffectbehaviorinanadaptivefashion, from the anterior pituitary and of arginine vasotocin and isotocin
includingdailyandseasonalextremesinactivity. (AVT/IT; arginine vasopression/oxytocin in mammals) from the
The motivation to reproduce, i.e., sexual arousal, activates posterior pituitary. Unlike the majority of vertebrates that have a
physiologicalprocessesthatcaneventually lead tosexualbehavior, blood portal system linking POA gonadotropin-releasing hormone
inclusive of hormonal, genetic and neural-dependent mechanisms (GnRH)neuronsandtheanteriorpituitary,theGnRHPOAneuronsin
(SchoberandPfaff,2007).Themajorpremiseofthisarticleisnotto teleostsdirectlyinnervatethepituitary(PeterandFryer,1983).This
re-review activational effects of steroid hormones or peptides on directpathwaymaybeaneuro-hormonaladaptationamongteleosts
reproductivebehaviorinfishes(e.g.,BassandForlano,2008;Godwin, allowing for rapid shifts in reproductive function (see Bass and
2010;OliveiraandGonçalves,2008),butrathertohighlightexamples Forlano, 2008 for more discussion). For instance, in the cichlid fish
wheretheneurochemically-rich coreof thecentralnervoussystem Astatotilapiaburtoni,sociallydominantterritorialmalesaretheonly
interacts with specific sensory and motor systems underlying ones that reproduce. When given the opportunity to become
reproductively motivated behaviors. We focus our discussion on dominant,asubordinatemalewillrapidly(withinminutes)change
twogroupsoffishes,teleostsandelasmobranchs.Jawedvertebrates its behavior. Within 30 minutes, neurons show an upregulation of
include bony and cartilaginous fishes (Fig. 1) (Nelson, 2006). Bony the immediate early gene egr-1 in POA areas of high GnRH-1
fishes are divided into two major clades, Actinopterygii and expression(Burmeisteretal.,2005).Thephysiologicalpropertiesof
Sarcopterygii. The majority of actinopterygians are teleosts, the GnRH neurons are also significantly different between territorial
largestgroupofliving vertebrates withat least30,000species,and males and non-territorial males, which likely translates into less
the principal focus of this review. Sarcopterygians include lungfish gonadotropin release in non-territorial males (Greenwood and
(Dipnoi),coelacanths(Coelacanthimorpha,Latimeria),andtetrapods Fernald,2004).ThereaderisreferredtoBassandGrober(2009)for
(we are all fishes!) (Fig. 1). The more basal cartilaginous fishes a recent discussion of the diversity in organization of the POA in
(Chondrichthyes) include holocephalans (chimaeras/ ratfish) and relationtotheremarkablerangeofreproductiveplasticityexhibited
elasmobranchs(sharks,skatesandrays). byteleostfishes.
ThepresenceofthenonapeptideAVT/AVPinmagnocellularand
Whatisknownoftheneuralcircuitryof“sexualarousal”infishes? parvocellular neurons of the POA in all vertebrates exemplifies the
conservedevolutionoftheneurochemicalcoreofthebrainoverthe
Connectivity, neurochemistry and function of the POA/anterior last500millionyearsormore.Furthermore,inalljawedvertebrates,
hypothalamus neuropeptide-containing neurons in the POA project to similar
extrahypothalamicbrainregionsincludingtheventraltelencephalon,
ThePOAandanteriorhypothalamus,neurochemical“core”areas midbraintegmentum,periaqueductalgray,andviscerosensoryareas
essential for the control of reproductive physiology and hence ofthemedulla(GoodsonandBass,2001;Saitoetal.,2004).AVT/AVP
behavior in all vertebrates, show a highly conserved pattern of iswelldocumentedinitsroleinmediatingvertebratesocialbehavior
anatomical organization (Butler and Hodos, 2005; Meek and (Goodson and Bass, 2001), including AVT manipulations affecting
Nieuwenhuys, 1998). The POA and anterior hypothalamus can be malereproductivedisplaysinteleosts(Carneiroetal.,2003;Saleket
viewed as one functional unit, the POA, because of their shared al., 2002; Santangelo and Bass, 2010; Semsar and Godwin, 2003;
developmental origin (Puelles, 2001) and obvious homologies Semsaretal.,2001).Inmammals,malepenileerectionisregulatedby
betweenneuropeptide-containingcellgroupsinthePOAofteleosts androgenic stimulation of oxytocin neurons in the paraventricular
(e.g., see Goodson et al., 2003) and the anterior hypothalamus of hypothalamus(PVN)(ArgiolasandMelis,2005).Themagnocellular
tetrapods(e.g.,theparaventricularandsupraopticnuclei)(seeBass nucleusofthePOAinteleostsisthoughttobethePVNhomologue,in
andForlano,2008forfurtherdiscussion). partduetoitsabundanceofAVT/ITneurons(Gilchriestetal.,2000;
TheroleofthePOAinbrainandbehavioralarousalisexemplified Kapsimali et al., 2001; see Forlano and Cone, 2007 for further
by its role as a sensorimotor integration center. Its motor outputs discussion).Likemammals,theselargeneuroendocrineneuronsalso
includeconnectionswithboththesomaticandvisceralmotorsystems project to the spinal cord in teleosts (Demski and Sloan, 1985;
Fig.1.Cladogramoflivingjawedvertebrates.AdaptedfromMaetal.(2010).
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618 P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629
Fig.2.Organizationalsummaryofvertebratesomaticmotor,visceralmotorandneuroendocrinesystems(fromBassandForlano,2008).Theadrenalcortexreleasesglucocorticoids
andmineralcorticoids,whiletheadrenalmedullareleasescatecholamines,includingepinephrineandnorepinephrine.SeeBentley(1998)forneurochemicaldetails.Reprintedwith
permission,CambridgeUniversitypress.
GoodsonandBass,2000b;GregoryandTweedle,1985;seeMeekand bothmalesandfemalesbystimulationofthecentralnucleusofthe
Nieuwenhuys, 1998; Prasada Rao et al., 1987) and therefore may dorsaldivisionofthetelencephalon(Dc),eventhoughfemalesnever
servetomodulatemotorbehaviorsassociatedwithreproduction(e.g., show this behavior in nature. Thus, sex differences in circulating
spermrelease;DemskiandKnigge,1971). androgens and/or androgen receptor expression in Dc or POA may
There is a large literature on the great diversity and plasticity of account for this sexually dimorphic behavior. Autoradiographic
hormonalcontrolofreproductivebehaviorinteleostfishes(seeBass studies of bluegill show testosterone- concentrating cells in the
and Grober, 2009; Godwin, 2010; Munakata and Kobayashi, 2010; POA,butnotinDc(Demski,1978).However,moresensitivemeasures
OliveiraandGonçalves,2008).However,withtheexceptionofvocal ofandrogenreceptor(AR)bindingsites,suchasinsituhybridization,
fish(seelatersection),littleiscurrentlyknownabouttheanatomyand mightrevealARmRNAexpressioninDc,ashasbeenshownintwo
physiologyofneuralcircuitryunderlyingthosebehaviors.Manystudies otherteleostspecies(Table1;Forlanoetal.,2010;Harbottetal.,2007;
highlight the diversity of neuropeptide phenotypes in the POA in MunchrathandHofmann,2010).Interestingly,testosterone-stimula-
relation to male social status and reproductive displays. Generally, tionofthePOAin malerodents alsoevokesnest-building behavior
territorial,displayingmaleshavemoreorlargerGnRH-immunoreactive (Fisher,1956).
(ir) cells, while AVT-ir/mRNA relationships are species-specific (for
reviewsseeBassandForlano,2008;BassandGrober,2001;Foranand
Bass, 1999; Godwin, 2010; Hofmann, 2006; Oliveira and Gonçalves, GnRHintheterminalnerveganglion
2008;Oliveiraetal.,2005).Thereareevenfewerfunctionalstudiesof
theteleostPOA(orotherbrainareas)inregardstosexuallymotivated TeleostshavetwoorthreeformsofGnRHinthreedistinctbrain
behavior (but see below and discussion on vocal fishes). AVT-ir and areas:thePOAwhichdirectlycontrolsgonadotropinreleasefromthe
GnRH-ir and/or their receptors are also found in peripheral sensory pituitary, as well as more poorly understood populations in the
organsandcentralsensoryprocessingareas(Dewanetal.,2008;Foran midbraintegmentumandganglionoftheterminalnerve(TN),both
et al., 1997; Goodson and Bass, 2000b; Grens et al., 2005; Maruska, thoughttoserve a neuromodulatory role in thebrain (review:Kah
2009;MaruskaandFernald,2010;MaruskaandTricas,2007;Stelletal., et al., 2007). TN neurons are typically clustered near the olfactory
1987),implicatingtheroleoftheseneuropeptidesinmodulatinglevels bulb-telencephalonjunctionandhavedirectprojectionstoboththe
of“sensoryresponsiveness”. retinaandolfactoryepithelium(DemskiandNorthcutt,1983;Kahet
Sexualbehaviorinfishes,likeothervertebrates,isoftenstimulated al.,2007;SchreibmanandMargolis-Nunno,1987).OkaandMatsush-
by olfactory/pheromonal, visual and auditory sensory stimuli or a ima(1993)characterizedtheoscillatory-likepropertiesofTNneurons
combination of these cues (for review, see Oliveira and Gonçalves, inthedwarfgourami,Colisalalia,andhypothesizedamodulatoryrole
2008;alsoseeSatouetal.(1994)forvisualandvibrational cuesin based on the TN's physiological properties and widespread projec-
salmon).AllofthesesensorysystemshaveinputstothePOAinfishes tionsthroughoutthebrain,includingtheolfactorybulbs,opticnerves,
(e.g.,Bassetal.,2000;Becerraetal.,1994;MeekandNieuwenhuys, hypothalamus, optic tectum, and spinal cord. Lesion of the TN
1998),againpointingtothePOAasamajorcentralintegrationsitefor depletes GnRH in the brain and negatively affects the frequency of
sensory cues and reproductive behavioral output. Early studies by nest building, a sexually motivated behavior stimulated by the
DemskiandKnigge(1971)demonstratedthatmultiplereproductive presence of a receptive female (Yamamoto et al., 1995). In Nile
behaviorsincludingnestbuilding(sweeping)andcourtshipcircling, tilapia, Oreochromis niloticus, removal of the olfactory epithelium
and an inhibition of aggression, as well as sperm release could be preferentially decreased nest building behavior as well as the
inducedinfreelyswimmingbluegillsunfishbyelectricalstimulation transcriptsencodingGnRH-1(TN)andGnRH-2(midbrain),probably
ofthePOA.Similarexperimentsinhimesalmon,Onchorhyncusnerka, byinteractionswithsecondorderolfactoryprojections(Uchidaetal.,
confirmed the POA as a control center for sexual behavior, both 2005). In Japanese medaka, Oryzias latipes, exposure to male visual
appetitiveandspawning(Satouetal.,1984).Interestingly,sweeping cues suppressed the electrical activity of female TN GnRH neurons.
behaviorinbluegillsunfish(Lepomismacrochirus)couldbeinducedin Interestingly,samesexandolfactorycuesingeneralhadnoeffecton
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P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629 619
Table1
Comparativedistributionofandrogenreceptor(AR),aromatase(estrogensynthase)andestrogenreceptor(ERα,ERβ1,ERβ2)transcriptsandestrogenandandrogenconcentrating
cellsintheforebrainofteleostswithputativemammalianhomologiesandmajornodesofthevertebratesocialbehaviornetwork(*).
Brainarea AR ([3H]T/DHT) Aromatase ERα ERβ(1/2) ([3H]E2) Putativemammalianhomologue
Ventraltelencephalon
Olfactorybulb(OB) a – m,t,z,p m,a a NR
Ventralnucleus(Vv)*Aud a p m,t,z,p m,a,s a,s t,p,x Septum2,11,16
Supracommissuralnucleus(Vs)*Aud,Voc m,a t m,t,z,p m,a a t,g,x Basalamygdala2,11
Postcommissuralnucleus(Vp)Aud m,a - m,t,z,p m,a,s a t Basalamygdala2,11
Dorsalnucleus(Vd) m,a NR m,t,z,p a,s a,s NR Striatum/basalganglia10,15,16
Intermediatenucleus(Vi) m (t) m,NR – – NR Basalamygdala13
Dorsaltelencephalon
Centralzone(Dc) m,a NR m,NR m,a a NR Pallialamygdalaordorsalpallium1,12,18
Centralmedialdivisionofmedial m,a NR m,t,z,p m,a a NR Pallialamygdalaordorsalpallium1,2,12,14,16,18
zone(Dm-cm)
Posteriordivisionofmedialzone m NR m,NR m NR “
(Dm-p)Aud,Voc
Dorsalposteriorzone(Dp) a t m,z m,a a – Piriformcortex10,11,12
Preopticarea*
Anteriorparvocellular(PPa)Aud,Voc m,a,z t,s,p,g,x m,t,z,p m,a,z,t,c,e,s,p a,c,z,p,s g,t,p,x POA7,9
Posteriorparvocellular(PPp)Aud,Voc m,a,z – m,t,z,p a,s,t,c,p a,s t POA7,9
Magnocellular(PM/PMg) m,a t,p,g,x m,t,z,p m,a,t,s,c,p a,c,s g,t,p,x Paraventricularnucleus5,6,8
Ventralhypothalamus
Anteriortuberal(AT)*Aud,Voc m,a NR m,t,z m,a,s,t,c a t Ventromedialhypothalamus4,7
Ventraltuberal(vT)*Aud,Voc m,a NR m,z a,NR a,NR NR Anteriorhypothalamus7
Periventricular(Hv/Hd) m,a,z t,m,s,p,g,x m,t,z,p m,a,s,c,e,z a,c,z,p,s g,t,p,x Arcuate3,5
Thalamus
Centralposteriornucleus(CP)Aud m,a NR m,z m,a,s a NR
Dorsalposterior(DPo) m,a NR m,t,z,p m,a,s a NR
Nucleuspreglomerulosus(PGl/m)Aud m,a t m,z a,s a t
Periventricularnucleusofposterior m,a,z – m,t,z m,a a,s t
tuberal(TPp)
Posteriortuberalnucleus(TP) m,a,z m m,t,z a,c,z,t a,c,z,s – Ventraltegmentalarea/substantianigra15,16
Pineal – NR m,NR m,NR NR NR
m=midshipman,Porichthysnotatus(Forlanoetal.,2001,2005,2010).
z=zebrafishDaniorerio(Gorelicketal.,2008;Menuetetal.,2002,2005).
t=trout,Oncorhyncusmykiss(Menuetetal.,2001,2003).
a=cichlid,Astatotilapiaburtoni(Harbottetal.,2007;MunchrathandHofmann,2010).
c=croaker,Micropogoniasundulatus(Hawkinsetal.,2005).
p=pejerrey,Odontesthesbonariensis(Strobl-Mazzullaetal.,2008).
s=seabass,Dicentrarchuslabrax(Muriachetal.,2008a,b).
e=eelpout,Zoarcesviviparous(Andreassenetal.,2003).
t=oystertoadfish,Opsanustau(Fineetal.,1996).
m=mormyrid,Brienomyrusbrachistius(Bassetal.,1986).
s=sunfish,Lepomiscyanellus(Morrelletal.,1975).
p=paradisefish,Macropodusopercularis(Davisetal.,1977).
g=goldfish,Carassiusauratus(Kimetal.,1978).
x=platyfish,Xiphophorusmaculatus(Kimetal.,1979).
NR=notrecorded.
Aud,Voc=definedauditoryandvocalnucleiinmidshipman.
1(Braford,1995);2(BruceandBraford,2009);3(Cerda-Reverteretal.,2003);4(Forlanoetal.,2005);5(ForlanoandCone,2007);6(Gilchriestetal.,2000);*7(Goodson,2005);
8(Kapsimalietal.,2001);9(MooreandLowry,1998);10(MuellerandWullimann,2009);11(Northcutt,1995);12(Northcutt,2006);13(NorthcuttandBraford,1980);14
(Portavellaetal.,2004);15(RinkandWullimann,2001);16(WullimannandMueller,2004);18(Yamamotoetal.,2007).
modulating TN GnRH activity in this species (Ramakrishnan and mechanisms (likely involving the POA) as injections of the prosta-
Wayne,2009). glandinPGF2αinthepreopticrecessofthethirdventricleoffemale
goldfisheffectivelytriggerthisbehavior,althoughtheexactmecha-
Olfactorypathwaysandsexualbehavior nismandsiteofactionisunknown(StaceyandPeter,1979).While
PGF2α is essential for female sexual behavior, estrogens are not.
Aroleforpheromonesinmaleandfemalereproductivebehavior PharmacologicalincreasesordecreasesinbrainGnRHconcentration
has been especially well documented by Stacey, Sorensen and will enhance and inhibit female spawning behavior, respectively
colleagues in goldfish (Carassius auratus) (Kobayashi et al., 2002; (VolkoffandPeter,1999).However,GnRHwithintheterminalnerve
Munakata and Kobayashi, 2010; Stacey and Liley, 1974; Stacey and ganglionappearstofunctionasa“potentiator”tofacilitatebehavior,
Sorensen, 2002). Prior to ovulation, females produce a progestin but is not essential as transection of the terminal nerve within the
17α,20β-dihydroxy-4-pregnen-3-one (17,20-P) in the ovarian folli- olfactory tract only increases the behavioral latency (see Munakata
cles that induces oocyte maturation. This progestin functions as a and Kobayashi, 2010). While gonadal steroids do not seem to be
“pre-ovulatorypheromone”thatinducesanLHsurgeinthemaleand necessaryforfemalereproductivebehavior,malesrequireandrogens
subsequentchasingbehavior(Dulkaetal.,1987).Prostaglandinsare (the teleost-specific androgen 11-ketotestosterone/11kT; Bentley,
produced in the ovary after ovulation and trigger female sexual 1998;Borg,1994)toprimecircuitryneededtorespondtothefemale
behavior (e.g., oviposition) that is thought to occur via central pheromonestimulus.Infact,androgensincreaseolfactoryresponsein
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620 P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629
males to female pheromone (15K PGF2α) measured by electro- interferedwithcriticalolfactory(pheromonal)processingnecessary
olfactogram(Cardwelletal.,1995).Interestingly,goldfishadultscan forsexualmotivation.Anatomicalstudieshavedemonstratedrecip-
bebehaviorallysex-changedbyprostaglandininjectioninamaleor rocalconnectionsofVsandtheolfactorybulbs,andinputtoVsfrom
11kT implant in a female followed by 15K PGF2α stimulation other olfactory bulb targets (Vv, Vd, POA, posterior tubercle in the
(Kobayashi et al., 2002). This example in goldfish, along with nest diencephalon;DemskiandNorthcutt,1983;MeekandNieuwenhuys,
buildinginbluegillsunfish(seeabove),andmale-femalereversalsin 1998; Shiga et al., 1985a). It is noteworthy that all of the above
sex-changing fishes (see Bass and Grober, 2009) implies bisexual mentionedareasaretargetsofsteroidhormonereceptorexpression
circuitryunderlyingsexualbehavioracrossdiversespeciesthatcanbe anddopaminergicinput(seeTable1,Fig.3andbelow).Inaddition,
simply activated under a sexually dimorphic hormonal or chemical lesionstotheanteriorPOA,andthelateralormedialforebrainbundle
signal(e.g.,androgens,prostaglandins). greatlyimpairmalesexualbehaviors(Koyamaetal.,1984).ThePOA
Teleosts havea directconnectionfrom theolfactory bulb tothe alsoreceivesinputfromVv,Vdanddiencephalicnucleiincludingthe
POA(anteriorparvocellular)andtothecatecholamine-richposterior ventralperiventricularhypothalamus(Hv/NLT)andanteriortuberal
tuberalnucleusinthecaudaldiencephalon.Othersecondaryolfactory nucleus(MeekandNieuwenhuys,1998;Shigaetal.,1985b),proposed
terminal fields that are consistent across teleost species include homologues of the mammalian arcuate and ventromedial hypotha-
putativehomologuesofthelateralseptum(Vv,ventralnucleusofthe lamicnucleus,respectively(Cerda-Reverteretal.,2003;Forlanoand
ventraldivision(V)ofthetelencephalon),amygdala(Vs,supracom- Cone,2007;Forlanoetal.,2005;Goodson,2005).
misuralnucleusofV),andstriatum(Vd,dorsalnucleusofV),aswell
as nucleus taeniae and the piriform cortex homolog (Dp, posterior Neurochemicalarousalpathwaysinthe“paracore”
nucleus of the dorsal division of the telencephalon) (see Meek and
Nieuwenhuys, 1998; homologies: Mueller and Wullimann, 2009; The median and laterally positioned “paracore” regions include
Northcutt,1995,2006;WullimannandMueller,2004).Electrophys- conserved dopamine, norepinephrine, and serotonin-containing
iological evidence for the POA as an integration site for olfactory neurons(Nieuwenhuysetal.,1988),neuromodulatorsthattogether
processing in teleosts was demonstrated by the activation of withhistamineandacetylcholineascendingpathwaysareknownto
parvocellular POA neuronsby electricalstimulationof theolfactory increase arousal in mammals (Kapp and Cain, 2001). The neuroan-
tractinsunfish(Hallowitzetal.,1971).Studiesfromadiverserangeof atomicaldistributionofthesepathwaysinfishesarewelldocumented
species (e.g., catfish, goldfish, cod, weakly electric fish, winter acrossseveraltaxaandinmanycasesshowaconservedpatternwith
flounder) have demonstrated that olfactory bulbs also receive tetrapods(Fig.3;KaslinandPanula,2001;Rodriguez-Moldesetal.,
reciprocalinputfromtheventralanddorsalposteriortelencephalon 2002a;SmeetsandGonzalez,2000;WullimannandMueller,2004).
and from a subset of Dc neurons (Bass, 1981; Levine and Dethier, Tract tracing studies in combination with tyrosine hydroxylase
1985;PrasadaRaoandFinger,1984;Sasetal.,1993;seeMeekand immunocytochemistry revealed an ascending activating system
Nieuwenhuys, 1998). In some species, the POA and monoamine- projecting from diencephalic posterior tuber neurons to septal and
containing areas such as the posterior tuberal, locus coeruleus and striatalhomologuesintheventraltelencephalon(Vv/Vd)inzebrafish
raphenucleiwerealsofoundtoprojecttotheolfactorybulb(Levine (Daniorerio)(RinkandWullimann,2001).Otherafferentstothisarea
andDethier,1985;PrasadaRaoandFinger,1984;Sasetal.,1993).The oftheventraltelencephalonarisefromcellgroupsknowntoexpress
medial olfactory tract, which projects largely to the ventral telen- serotonin, acetylcholine and histamine (Bellipanni et al., 2002;
cephalon, includes the projections of the GnRH neurons in the Clementeetal.,2004;KahandChambolle,1983;KaslinandPanula,
terminalnerveganglionthatarethoughttopreferentiallyencodesex 2001;Margolis-Kazanetal.,1985;Perezetal.,2000).
pheromones (Demski and Northcutt, 1983; Dulka, 1993; Sorensen In teleosts, a midbrain tegmental population of dopaminergic
etal.,1991). neuronsismissing,butaposteriortuber-Vdpathwayishypothesized
SeverallesionstudiesofVsand/orposteriorVvhavesubstantiated to be homologous to the nigro-striatal pathway in mammals since
theirimportanceinmalecourtshipandspawningbehavioringoldfish somemammaliandopaminergic(substantianigra)neuronsarefound
and other species (Koyama et al., 1984; Kyle and Peter, 1982; Kyle intheembryonicbasaldiencephalonand,likezebrafish,expressthe
et al., 1982). Kyle and Peter (1982) hypothesize that the lesions Nurr1 gene and are developmentally regulated by the nr4A2 gene
Fig.3.Ascendingactivatingsystemstotheventraltelencephalonintheadultzebrafishbrain(modifiedfromWullimannandMueller,2004;permissionfromWiley-Liss,Inc.).
Double-labelingstudiesidentifiedtheposteriortuberculum(PT)todorsalnucleusoftheventraltelencephalon(Vd)projection,proposedashomologoustothemeso-striatalpathwayin
mammals.Cholinergic(superiorreticular),serotonergic(superiorraphe),andhistaminergic(caudalhypothalamic)nucleirequireneurochemicalconfirmation.Ha,habenula;TL,torus
longitudinalis;Vs,supracommisuralnucleus;Vvventralnucleusoftheventraltelencephalon.
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P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629 621
(Kapsimalietal.,2001;Luoetal.,2008;RinkandWullimann,2001, nin-containing raphe nucleus, and less so the noradrenergic locus
2002).Interestingly,cartilaginousfishes(elasmobranchs,e.g.,sharks coeruleusand histaminergic neuronsin theventrocaudal hypothal-
and rays) have both midbrain and posterior tuber dopaminergic amus.Onlymoderatecontactsweremadetomesopontinecholinergic
groups(MeredithandSmeets,1987;Stuesseetal.,1990),suggesting neurons, but all the above systems showed evidence of reciprocal
teleostsareexhibitingaderivedcondition(WullimannandMueller, connectionswithorexin-containingneuronsinthePOA(Kaslinetal.,
2004). In general, the widespread neuroanatomical distribution of 2004).Theseneuroanatomicalstudiessuggestthatdailyrhythmsin
tyrosinehydroxylase-irneuronalgroupsandfiberprojectionsarewell general arousal provided by orexin may, in turn, directly activate
documented in diverse taxa of fishes (for review, see Smeets and circuits involved in sexual behavior (e.g., POA; striatal and septal
Gonzalez,2000),andareinlargepartfoundinpredictedregionsthat homologues)orindirectlybymodulatingascendinganddescending
correspondtoputativemammalianhomologues. aminergic systems (Kaslin and Panula, 2001; Kaslin et al., 2004). A
Teleosts contain adrenergic neurons in the locus coeruleus and study in goldfish found fewer orexin-ir contacts with aminergic-
caudal medulla, and dopaminergic diencephalic populations in the containingneuronsinthetegmentumcomparedtothatreportedin
hypothalamus(includingPOA),ventralmedialthalamusandventral zebrafish(Huesaetal.,2005);thus,furtherstudieswithotherspecies
telencephalon(e.g.,Filippietal.,2010;Ma,2003;McLeanandFetcho, and localization of orexin on aminergic neurons at the subcellular
2004;RinkandWullimann,2001;SmeetsandGonzalez,2000).Like levelmayclarifythefunctionalsignificanceofpotentialinterspecific
tetrapods,thereisadensetyrosinehydroxylase-irsomatapopulation variation. In rodents, there is evidence that orexins may integrate
intheolfactorybulbsandretinaaswellasrobustfiberswithinsensory motor activity associated with motivated (reward) behaviors by
integration centers such as the optic tectum and the olfactory- modulatingtheascendingdopaminergic system (seeScammell and
recipient posterior dorsal telencephalon (Dp) (Meek and Nieuwen- Saper, 2005); future explorations of these interactions in fishes are
huys, 1998). While dopamine is well documented as a regulator of also potentially fruitful areas for investigation of neuromodulatory
reproductioninteleostsbyinhibitinggonadotropinreleaseincertain mechanismsofsexualmotivation.
species (Dufour et al., 2005; Zohar et al., 2010), little is known
regarding its function in sexually motivated behaviors as is well Steroidhormonereceptorsincircuitsinvolvedinreproductivebehavior
definedinrodents(Hulletal.,2004).However,basedonitsconserved
neuroanatomical distribution and connectivity with brain areas It is beyond the scope of the present essay to review the vast
involvedinsexualbehavior,aswellasevidencethatpharmacological literatureofactivationaleffectsofsteroidhormonesonreproductive
manipulationsofdopaminecanaffectrewardcircuitryandmotiva- behavior in fishes (for comprehensive reviews see Godwin, 2010;
tion (DarlandandDowling,2001; LettandGrant, 1989), it islikely OliveiraandGonçalves,2008;Oliveiraetal.,2005).Rather,weprovide
dopamine plays a similarly important role in sexual motivation in whatisknownregardingthedistributionof(sex)steroidreceptorsin
fishes. the central and peripheral nervous system of teleosts, highlighting
Monoamines are also documented to regulate neuropeptides in areas discussed in the text that are directly linked to reproductive
the core of the reproductive axis of the teleost brain. Chronic behaviors and/or nuclei that contain ascending arousal pathways.
treatment by fluoxetine, a serotonin reuptake inhibitor, decreases Table 1 shows a comparison of androgen and estrogen receptor
AVTmRNAexpressioninthePOA,aswellasaggressivebehaviorin expression,steroid-concentratingcells,andtheestrogen-synthesizing
dominant,courtingblueheadwrassemales(Thalassomabifasciatum) enzymearomataseinteleostforebrainnucleiandproposedmamma-
(SemsarandGodwin,2004).Fluoxetinetreatmentoffemalegoldfish lianhomologuesifknown.Alsoindicatedinthetableisexpressionof
dramaticallydownregulatesisotocin(oxytocinhomologue)andERβ1 steroid receptors in major nodes of the “vertebrate social behavior
mRNAinboththehypothalamusandtelencephalonandERαinthe network” in fishes (i.e., med amygdala/ BnST (Vs); lateral septum
telencephalon,andalsodecreasesplasmaestradiollevels(Mennigen (Vv); ventromedial hypothalamus (AT); POA; PAG not listed in
et al., 2008). Within the POA, noradrenergic activity increases and Table1butseeFig.4)(Goodson,2005).Notsurprisingly,likeallother
serotonergicactivitydecreasesduringfemaletomalesexchangein vertebrates, receptors for androgens and estrogens are robustly
the saddleback wrasse, Thalassoma duperrey, changes paralleled expressed in the POA and hypothalamus in teleosts. Thus, steroid
within the locus coeruleus and raphe nucleus, respectively (Larson receptors are localized within conserved brain areas that control
et al., 2003b). Experimentally increasing norepinephrine levels or reproductive behavior and/or contain various modulatory peptides
decreasingserotoninlevelscanfacilitatesexchange,whiletheinverse that regulate arousal. Unlike mammals, little is known about
treatmentsinhibit sex change in this species (Larson et al., 2003a). progesteronereceptor(PR)inbrain,orroleofprogesteroneinsexual
Investigatingdopaminergicandserotonergicsystemsinfishesinthe behaviorinfishes,however,asexpected,itisrobustlyexpressedin
contextofsexualarousalandtheirinteractionswithotherneuropep- thePOA(Hannaetal.,2010;MunchrathandHofmann,2010).
tidesremainsaninterestingcomparativetopicforfurtherstudy. While the importance of gonadal steroids on male and female
Thehistaminergicsystemregulatesgeneralbrainarousalindaily reproductive behavior is quite variable across teleosts (Borg, 1994;
behavior and physiology, including circadian rhythms of locomotor Munakata and Kobayashi, 2010; Oliveira and Gonçalves, 2008) and
activity, waking, and feeding (Wada et al., 1991). Since histamines sexual behavior in some fishes has been demonstrated to be
havestimulatoryandinhibitoryeffectsonserotonin,noradrenaline, independent of gonadal steroids (Godwin et al., 1996; Kobayashi
dopamineandacetylcholineinmammals(Schlickeretal.,1994)and andStacey,1993;SemsarandGodwin,2003),thebrainaswellasthe
have widespread reciprocal connections in teleosts (Kaslin and gonadsarebothlikelysourcesofsteroidhormoneswhichmodulate
Panula, 2001), these complex interactions provide a rich potential theneuralcircuitscontrollingreproductivebehavior;gonadalsteroids
foruncoveringbrainandsexualarousalinfishandothervertebrates. alsomayfunction,inpart,toupregulateneurosteroidproductionin
In addition, orexin (hypocretin) neurons, another hypothalamic the brain (e.g., Forlano and Bass, 2005; see reviews in Diotel et al.,
peptidergicsysteminvolvedinarousalstates(suchaswakefulness), 2010;Forlanoetal.,2006).Highlevelsofbrainaromataseinteleosts
werefoundinzebrafishtohavelargelysimilarprojectionpatternsas (the highest among all vertebrates) may regulate the ratio of
mammals, including innervation of striatal (Vd) and septal (Vv) androgens to estrogens that reach behavioral circuits on a rapid or
homologues and the periventricular hypothalamus. Additionally, long-term timescale (Forlano et al., 2006; Bass and Forlano, 2008;
unlike mammals, an orexin-like cell population was found in the also, see discussion below for vocal fishes). For instance, within
magno- and parvocellular POA. Interestingly, orexin-ir fibers also minutestohoursafterfemaletomalesexchangeinthebluebanded
densely innervated diencephalic dopaminergic neurons (thought goby,Lythrypnusdalli,anincreaseinaggressivebehavioranddecrease
homologous to the mammalian ascending system) and the seroto- inbrainaromataseactivityoccurs(Blacketal.,2005).Inmalegoldfish,
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622 P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629
Fig.4.Sideviewsofthebrainshowingvocalmotor(A)andauditory(B)systemsinbatrachoididfish(midshipmanandtoadfish)(adaptedfromForlanoetal.,2010).Soliddots
representsomata,andlinesrepresentaxonalprojectionpathways.Twoconnecteddotsindicatereciprocalconnections.Shadedareasindicatelocalizationofsteroidhormone
receptormRNA(1,androgen;2,estrogenalpha),aromatase(3),andneuropeptideinnervation(4,argininevasotocin/isotocin)(seeForlanoetal.,2001,2005,2010;Goodsonand
Bass,2000b;Goodsonetal.,2003).A:Descendingvocalpathways.Preoptic(POA)andhypothalamicventral(vT)andanterior(AT)tuberalnucleiprojecttothemidbrain
periaqueductalgray(PAG)whichinnervates,inturn,thevocalpatterngeneratorcircuit(VPG)inthehindbrain-spinalcord.TheVPGconsistsofvocalprepacemaker(VPP),
pacemaker(VPN)andmotor(VMN)nuclei.VMNaxonsexitthebrainviaoccipitalnerveroots(likelyhomologuesofhypoglossal)tosound-producingvocalmuscleattachedtothe
swimbladder(ventralview).Alsoshownisarepresentative“grunttrain”vocalizationproducedbynestguardingmale.B:Centralauditorypathways.Vocalizations(e.g.,grunttrain)
aredetectedbyauditorysacculewithintheinnerearwhichprojectsviatheVIIIthnervetoauditorynucleiinthehindbrainthatinnervatetheauditorymidbraintorussemicircularis
(TS).ShownarenucleiinterconnectedwithTS.Adorsalthalamicnucleus(centralposteriornucleus,CP)containsreciprocalconnectionstothetelencephalon(dorsomedial/Dm)and
ventralsupracommissural/Vs)thatreceivesinputfromanteriorhypothalamus-posteriortubercle(fornomenclatureseeBrafordandNorthcutt,1983).TSandCPalsoconnectto
forebrain(anteriorhypothalamus,POA)andmidbrain(PAG,isthmal/tegmentum)vocalsites,whileauditory-recipienthindbrainnucleiconnecttothepatterngeneratingVPG
circuit(alsoseeBassetal.,1994;GoodsonandBass,2002).SeeForlanoetal.(2010)foradditionalbackgroundreferences.
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P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629 623
aromatase inhibition blocks the rapid effects of testosterone on motivationbypreviouslygravidfemalestoattendtoadvertisement
visually mediated approach behavior toward females (Lord et al., callsledtostudiesofshiftsinauditorysensitivitythatmightbelinked
2009).Inguppies,Poeciliareticulata,twoofthreemalesexualdisplays to this dramatic behavioral change. Subsequent investigations
were reduced by aromatase inhibition (Hallgren et al., 2006), showedseasonalandsteroid-dependentenhancementintheability
suggestingtestosteronearomatizationintoestradiolfacilitatesthese oftheperipheralauditorysystemtoencodethefrequencycontentof
behaviors. Nesting males of the peacock blenny, Salaria pavo, have the advertisement call (Sisneros, 2009; Sisneros and Bass, 2003;
higher brain aromatase activity than males that adopt a sneaking Sisnerosetal.,2004a).Whilethismechanismcanaccountforseasonal
reproductive tactic (Goncalves et al., 2008). Sex differences in changes in auditory encoding ability that parallel changes in
aromatase activity or expression in various brain regions including circulating steroid levels (i.e., steroids “prime” the auditory system
thePOAofteleostsisfoundinseveralspecies(reviewedinForlanoet toencodeadvertisementcalls),theneuralmechanismsleadingtothe
al., 2006; Goncalves et al., 2010; Goncalves et al., 2008), and thus suddenchangeinfemalephonotaxisremaintobeshown.Thesteroid
similarlevelsofcirculatingtestosteronebetweensexescouldbeseen dependent plasticity of auditory encoding is a specific example of
verydifferentlyinbrainareaswhereandrogenmetabolismissexually estrogen-induced peripheral nervoussystemarousal(Lee and Pfaff,
dimorphic. It is interesting to note that while the vast majority of 2008) that might be analogous to estrogen-dependent enlarging of
teleost fishes reproduce by external fertilization and estrogen does the genitosensory field of tactile receptors in rodents (Bereiter and
not appear necessary for female sexual behavior (Munakata and Barker,1980).
Kobayashi,2010),guppiesareinternalfertilizers,andlikemammals, Midshipman fish have two male reproductive morphs; type I,
female receptivity is regulated by estradiol (Liley, 1972). Although territorial/nesting males acoustically court females while type II,
mostfemaleteleostshavelowcirculatingestradiollevelsduringthe sneak/satellite spawning males steal fertilizations from the type I
spawningperiod(seeSisnerosetal.,2004bandreviewwithin),the malesduringspawningbehaviors(BrantleyandBass,1994).TypeI
productionofestrogenwithinthebrainitselfmaystillbehighand and II males diverge in a large suite of somatic, neural and
importantinregulatingfemalesexualbehaviorinsomespecies. neuroendocrine traits (for recent reviews see Bass and Forlano,
2008; Bass and Grober, 2009; Bass and Remage-Healey, 2008). The
Brainarousalandreproductivebehaviorinvocalfishes sensitivityofthecentralvocalcircuittothenonapeptidesAVT/ITand
steroids (androgens and glucocorticoids) shows both sex and male
Vocal teleost fish species have a long history as models for morph-specificvariation(GoodsonandBass,2000a;Remage-Healey
studyingtheneuralbasisofbehaviorduetotheirsimple,stereotyped, andBass,2004,2007).Thesteroidphenotypeparallelsmorph-specific
and easily quantified behaviors that are controlled by a discrete patterns in circulating levels of androgens and estrogen (Remage-
populationofneuronswhoseanatomicalandphysiologicalproperties HealeyandBass,2007).Aseriesoffieldstudiesofthecloselyrelated
arewelldefined(BassandZakon,2005).Thesefishhavealsoprovided toadfish(Opsanusbeta)showhowrapidshiftsincirculatingandrogen
excellent models to study how steroids and neuropeptides rapidly levelscanaccountforsimilarlyrapidchangesinnestingmalecalling
modulateplasticityinneuralcircuitscontrollingbehavior(Bassand behavior in response to behavioral playbacks of conspecific calls
Remage-Healey,2008;Forlanoetal.,2007;GoodsonandBass,2000a). (Remage-HealeyandBass,2005,2006).Themostrecentneurophys-
Inspeciessuchasthemidshipmanfish(Porichthysnotatus),wherethe iological studies show a nocturnal, reproductive dependence in the
productionandperceptionofsoundisessentialforreproduction(Bass ability of the central vocal network to generate long duration
andMcKibben,2003),wecanaskquestionsregardingthearousalof advertisement and aggressive calls that only type I males generate
sexualmotivationatthelevelofbothvocalandauditorycircuits,in during the breeding season (Rubow and Bass, 2009). A potential
themaleandfemale,respectively.Althoughmanyteleostsusesound modulatoryroleofpeptidergicandsteroidhormonesontheseevents,
communicationforcourtshipandaggressiveinteractions(e.g.,Ladich inthiscaseonadailybasis,seemslikelygiventheabovestudies.
etal.,2006;Maruskaetal.,2007;SantangeloandBass,2006;Simoes Together,theabovestudiesshowhowbothpeptidesandsteroids
et al., 2008), little is known regarding the neural pathways and have powerful modulatory influence over both vocal and auditory
mechanisms of sound production (and reception) outside of the mechanismsintoadfishes.GoodsonandBass(2002)outlinedmajor
toadfishfamily(Batrachoididae)thatincludesmidshipman. nodes of interface between the vocal–auditory network and the
Behavioral and neurophysiological studies demonstrate the ex- neuroendocrine axis, largely focusing on the projections of POA–
treme seasonal and daily rhythms of brain arousal related to social nonapeptidecontainingneurons(alsoseeGoodsonetal.,2003).The
vocal communication in midshipman fish, mechanisms that are integration of more recent studies showing the central expression
potently influenced by both peptidergic and steroid hormones. pattern of aromatase as well as estrogen and androgen receptors
Although not as well studied compared to hormone-driven male (Fig.4;Table1)nowrevealspatternsofbothpeptidergicandsteroid
courtshipbehaviorsinfishes,exampleswherefemalesactivelyseek receptor containing systems that are conserved across the major
outandchooseamalematearegoodmodelsforidentifyingbrain- vertebrate lineages and, more specifically, have co-evolved with
behavioral neuroendocrinological mechanisms underlying brain vocal-acoustic networks. Fig. 4 shows steroid receptors, aromatase
arousal and the motivation to reproduce. Midshipman females use and AVT/ITin vocal and auditory circuits in the midshipman brain.
theadvertisementcallsofmalestofindtheirnestsitesduringthelate Withthesemapsinplace,neurophysiologicalstudiescannowmore
spring-summerbreedingseason(BrantleyandBass,1994;McKibben fully explore how neuroendocrine signaling pathways modulate
andBass,1998).Underwaterplaybacksshowthatfemalesdistinguish vocal–auditory neuronal integration that leads to changes in brain
between calls based on their frequency, duration, amplitude and arousal levels related specifically to vocal-acoustic behaviors and
patternsofamplitudemodulation(McKibbenandBass,1998,2001), moregenerallytoseasonalpatternsofreproduction.
traitsencodedbycentralauditorypathways(seeBassandMcKibben,
2003). Only females filled with mature eggs (i.e., gravid) show a Neuralsubstratesforsexualarousalandreproductivebehaviorin
positive phonotactic response to advertisement calls. Once females elasmobranchfishes
releasealloftheireggs,theyleavethenestandmalesremaintoguard
developingembryos/larvae(BrantleyandBass,1994);theyalsono Elasmobranchfishesareanimportantgroupforcomparativeand
longer respond to playbacks of advertisement calls (McKibben and evolutionary studies, as they belong to the oldest lineage of extant
Bass,1998).Femalephonotaxisbehavior,adirectedmotorresponse jawed vertebrates (Chondrichthyes, see Fig. 1), and serve as an
stimulatedbyasinglesensorymodality,isanunambiguousproxyfor outgroup to bony vertebrates (actinopterygians and tetrapods) and
high sexual arousal in this species. The apparent loss of any maythereforeprovidefurtherinsightsintotheancestralvertebrate
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624 P.M.Forlano,A.H.Bass/HormonesandBehavior59(2011)616–629
conditioninbrainandbehavior.Inmanyrespects,theirreproductive season(Tricasetal.,1995).Inananalogousexampletotheseasonal
physiology (Maruska and Gelsleichter, 2010) and, in some cases, plasticity and hormone regulation of the female midshipman
chemicalneuroanatomy(below)ismoresimilartomammalsthanto peripheralauditorysystem,thefrequencytuningofelectroreceptors
themorerecentlyderivedteleosts.Outofthealmost30,000speciesof inmaleAtlanticstingrays,Dasyatissabina,changeswiththenatural
teleosts, only a very small percentage exhibit internal fertilization cycling of circulating androgens (Tricas et al., 2000) and can be
(i.e.,thePoecilidfamily:guppies,swordtailsandplatyfish)(Nelson, inducedbyexperimentallyincreasinglevelsofserumdihydrotestos-
2006).Incontrast,allchondrichthyanshaveintromittentcopulatory terone(SisnerosandTricas,2000).Thesignificanceofthischangein
organs(claspers)derivedfromthemedialsectionofeachpelvicfin frequencytuningisthatthissensorymodalitybecomesoptimizedto
used for internal fertilization (Pratt and Carrier, 2001). Out of the detectthenaturalbioelectricfieldofthefemale(SisnerosandTricas,
approximate940speciesofelasmobranchs(Nelson,2006),themodes 2000; see Bass and Zakon, 2005 for recent review of comparable
ofreproductionarequitediverse:themajorityoftaxa(70%ofsharks steroid-dependent, electrosensory-motor coupling mechanisms
and all rays) are viviparous (livebearers) often with long gestation among teleosts). Unreceptive female round stingrays also use
periods where embryos receive placental or aplacental (e.g. yolk) electroreception to find each other, as they are found buried in
nourishment,tooviparous(egglaying)skates(Rajiformes),andsome groupsforrefugelateinthematingseason(SisnerosandTricas,2002;
small bodied sharks (Wourms and Demski, 1993). Documented Tricasetal.,1995).Thesestudiesandthoseinmidshipmanexemplify
reproductive behaviors in this group include complex interactions striking examples of adaptive coordination of natural seasonal
such as the establishment of dominance hierarchies, group mating, changes in reproductive steroid hormones that optimize sensory
andevencooperativebreeding(PrattandCarrier,2001,2005). responsivenesstolocatemates.
Interestingcomparativequestionsarisewhenoneaskshowmight Atlanticstingraysaredocumentedtohavethelongestcontinuous
themodeoftheactofreproduction(internalvs.externalfertilization) mating season (8–9months) of any elasmobranch (Kajiura et al.,
anditsevolutionaryadaptationsshapetheneuroendocrinecontrolof 2000; Maruska et al., 1996; Snelson et al., 1988); ovulation and
reproductivebehavioracrossvertebrates.Forinstance,aremechan- fertilizationoccurat least7monthsaftermatingbegins.Matingfor
ismsunderlyingsexualphysiologyandarousalinsharksandguppies long periods without fertilization may function to stimulate ova
more similar to each other and rodents than either are to other developmentinthisspecies(Maruskaetal.,1996).Theresultsparallel
teleosts?Whilesomestudiesinelasmobranchscorrelatecirculating studiesinmammalsthatindicatecopulatoryactivityisnecessaryin
steroid hormones with reproductive state, few have investigated somespeciesfortriggeringovulationorstimulatingneuroendocrine
hormonalandneuralmechanismsthatdirectlycontrolreproductive regulation of reproductive behavior such as estrogen-dependent
behavior. We summarize below some research on stingrays that release of oxytocin in spinal cord (Komisaruk and Steinman, 1986;
approaches this subject of sexual arousal from a behavioral, Sansoneetal.,2002).Kajiuraetal.(2000)proposedthatstimulation
neuroecological perspective. For a recent comprehensive review on of cutaneous receptors by male biting and grasping may trigger
chondrichthyan hormones and reproduction, see Maruska and reproductiveinductioninfemales.Dermalthickness,whichdoesnot
Gelsleichter(2010). varyseasonally,is50%greaterinfemales,andmayprotectthemfrom
Unlikesomemaleteleostswhichemploydramaticcolorchange, seriousinjuryduringthereproductiveseason(Kajiuraetal.,2000).In
intricateswimmingdisplaysandacousticsignalstocourtfemales,the addition,femalestingrayshavealowerdensityoffreenerveendings
precopulatory behaviors of elasmobranch males include following, withinthedermisonthediscmarginwherethegreatestproportionof
nosing,andaggressivetactileassaultsonthefemale,intheformof bite wounds is located. These receptors, which may encode
biting,andoralgrasping(reviewedinPrattandCarrier,2001),which mechanical stimuli are well positioned to transmit information to
was proposed as a releasing mechanism to facilitate female assess mate quality (e.g., size and strength of bite) (Callahan et al.,
cooperationin mating(Springer, 1960). Elevatedcirculating andro- 1999). Whether this sexual dimorphism is dependent on sex
gens(namelytestosteroneanddihydrotestosterone)arethoughtto differences in steroid hormone levels, or the sensitivity of these
driveaggressivecourtshipbehaviorinsomespecies(Rasmussenetal., receptors peak with serum estrogen levels around the time of
1999; Tricasetal., 2000). Theresultingwoundsthat appearonthe ovulation (Tricas et al., 2000), are interesting questions for future
femaleskinareareliableindicatorofreproductiveactivity(Kajiuraet investigationsthatmayrevealparallelswithestrogenmodulationof
al., 2000). Thus, for successful copulation, males must be highly thesomatosensory-inducedlordosisbehavior(Kowetal.,1979;Pfaff
motivated to seek out females (populations are often sexually et al., 1977) or enlargement of mechanoreceptive sensory fields in
segregated)andphysicallystimulatehertoreceptivity,generallyby femalerodents(BereiterandBarker,1980).
gripping the female pectoral fin in its jaws; receptive females may Ascending projection systems are remarkably conserved between
archtheirback,flareorcuptheirpelvicfinstoexposetheircloacato elasmobranchsandothervertebrates(Cruceetal.,1999;Ebbessonand
allowinsertionoftheclasperforfertilization(PrattandCarrier,2001, Hodde, 1981; Sneddon, 2004), including abundance of the natural
2005). However, females are often not receptive to the male's opioid, enkephalin (Snow et al., 1996; Stuesse et al., 1991a,b), and
advances and are instead highly motivated to avoid copulation by serotonergic(Carreraetal.,2008;Ritchieetal.,1983;StuesseandCruce,
strugglingfree,shieldingtheircloacaagainstthesubstrate,orfleeing 1992;Stuesse etal.,1995),catecholaminergic(MeredithandSmeets,
toareasnotconducivetomating(shallowwater)(PrattandCarrier, 1987; Stuesse and Cruce, 1992; Stuesse et al., 1990) and cholinergic
2001,2005).Thistypeofbehaviorsuggestsfemalematechoiceand neuronal groups (Anadon et al., 2000). As mentioned previously,
assessmentviastrongsomatosensorystimuli(seebelow). elasmobranchs exhibit an ascending dopaminergic system consistent
Some female elasmobranchs may have a more active role in withtetrapodsthatincludesaventraltegmental(A9–A10)dopaminer-
precopulatory behavior, as documented in skates, where females gic cell population (unlike teleosts) (Meredith and Smeets, 1987;
display back arching and pectoral fin undulations to attract males reviewedinSmeetsandGonzalez,2000).Whileelasmobranchs,teleosts
(LuerandGilbert,1985).Basedontheobservationthatmalesofsome and tetrapods contain catecholaminergic cell groups in the POA and
sharkspeciesfollowfemalescloselypriortocopulation,pheromones anteriorhypothalamus,elasmobranchsareagainsimilartomammals
are hypothesized to play a role in stimulating mating behavior (and different from teleosts) with the absence of catecholaminergic
(Demski, 1990; Heuter et al., 2004; Johnson and Nelson, 1978); neuronsin the pretectum andpresence in the habenula and cortical
however,atthistime,therearenoexperimentaldatatosupportthis. equivalentgroups(reviewedinSmeetsandGonzalez,2000).Further-
An elegant set of field experiments demonstrated that male round more, a comparison of cholinergic cell groups across vertebrates
stingrays,Urolophushalleri,utilizeelectroreceptiontopreciselyorient revealed patterns of highly conserved cell groups in the habenulo-
and pinpoint buried females for mating during the reproductive interpeduncularsystem,cranialandspinalmotornuclei,magnocellular