The effects of naloxone on courtship and pairing behaviour in male and female zebra finches: the importance of testing mechanisms using multiple paradigms

in Behaviour
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Opioids are implicated in social attachments, but their role in avian pair bonds is not well understood. The present study tested the effects of naloxone, an opioid antagonist, on pairing using both a forced-choice and a mixed-sex aviary paradigm. First, three doses of naloxone were systemically administered in males using a repeated measures forced-choice design, partner preference formation was tested on the second day. Males treated with 20 mg/kg sang less undirected song. Males treated with 10 mg/kg of naloxone sang less to the familiar partner than when treated with saline and were less likely to form a partner preference than were other treatments. In females, 10 mg/kg of naloxone in a forced-choice paradigm increased preference for the unfamiliar over the familiar male. Finally, males and females were administered either naloxone (10 mg/kg) or saline in a mixed-sex aviary. In females, naloxone increased pairing behaviours, but had no other effects in either sex. Our findings suggest that the effects of naloxone on pairing-related behaviours are context-dependent; male–male competition may decrease the effects of naloxone on male song and a choice of mates may increase affiliation in females in a semi-naturalistic paradigm, and increase preferences for an unfamiliar partner in a forced-choice paradigm. Our findings highlight the importance of using multiple paradigms to test mechanisms of behaviour. These findings contribute to our understanding of the mechanisms of monogamous relationships and suggest that opioids play a role in male courtship, female affiliation and partner preferences in both sexes of zebra finches, but that context is important.

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References

BurgdorfJ.PankseppJ. (2006). The neurobiology of positive emotions. — Neurosci. Biobehav. Rev. 30: 173-187.

BurkettJ.P.SpiegelL.L.InoueK.MurphyA.Z.YoungL.J. (2011). Activation of μ-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles. — Neuropsychopharmacology 36: 2200-2210.

Coria-AvilaG.A.SolomonC.E.VargasE.B.LemmeI.RyanR.MenardS.GavrilaA.M.PfausJ.G. (2008). Neurochemical basis of conditioned partner preference in the female rat: I. Disruption by naloxone. — Behav. Neurosci. 122: 385-395.

DunnA.M.ZannR.A. (1996). Undirected song encourages the breeding female zebra finch to remain in the nest. — Ethology 102: 540-548.

GravesF.C.WallenK.MaestripieriD. (2002). Opioids and attachment in rhesus macaque (Macaca mulatta) abusive mothers. — Behav. Neurosci. 116: 489-493.

GulledgeC.C.DevicheP. (1999). Age- and sex-related differences in opioid receptor densities in the songbird vocal control system. — J. Comp. Neurol. 404: 505-514.

HollowayK.S.CornilC.A.BalthazartJ. (2004). Effects of central administration of naloxone during the extinction of appetitive sexual responses. — Behav. Brain Res. 153: 567-572.

IsmailN.Girard-BeriaultF.NakanishiS.PfausJ.G. (2009). Naloxone, but not flupenthixol, disrupts the development of conditioned ejaculatory preference in the male rat. — Behav. Neurosci. 123: 992-999.

KalinN.H.SheltonS.E.LynnD.E. (1995). Opiate systems in mother and infant primates coordinate intimate contact during reunion. — Psychoneuroendocrinology 20: 735-742.

Kelm-NelsonC.A.StevensonS.A.CordesM.A.RitersL.V. (2013). Modulation of male song by naloxone in the medial preoptic nucleus. — Behav. Neurosci. 127: 451-457.

KeverneE.B.MartenszN.D.TuiteB. (1989). Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. — Psychoneuroendocrinology 14: 155-161.

KhurshidN.AgarwalV.IyengarS. (2009). Expression of μ- and δ-opioid receptors in song control regions of adult male zebra finches (Taenopygia guttata). — J. Chem. Neuroanatom. 37: 158-169.

KhurshidN.JayaprakashN.HameedL.S.MohanasundaramS.IyengarS. (2010). Opioid modulation of song in male zebra finches (Taenopygia guttata). — Behav. Brain Res. 208: 359-370.

Le MerrerJ.BeckerJ.A.BefortK.KiefferB.L. (2009). Reward processing by the opioid system in the brain. — Physiol. Rev. 89: 1379-1412.

MabryK.E.StreatfeildC.A.KeaneB.SolomonN.G. (2011). avpr1a length polymorphism is not associated with either social or genetic monogamy in free-living prairie voles. — Anim. Behav. 81: 11-18.

MartelF.L.NevisonC.M.RaymentF.D.SimpsonM.J.KeverneE.B. (1993). Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. — Psychoneuroendocrinology 18: 307-321.

MartelF.L.NevisonC.M.SimpsonM.J.KeverneE.B. (1995). Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. — Dev. Psychobiol. 28: 71-84.

MehraraB.J.BaumM.J. (1990). Naloxone disrupts the expression but not the acquisition by male rats of a conditioned place preference response for an oestrous female. — Psychopharmacology 101: 118-125.

MillerR.L.BaumM.J. (1987). Naloxone inhibits mating and conditioned place preference for an estrous female in male rats soon after castration. — Pharmacol. Biochem. Behav. 26: 781-789.

PankseppJ.HermanB.ConnerR.BishopP.ScottJ.P. (1978). The biology of social attachments: opiates alleviate separation distress. — Biol. Psychiatr. 13: 607-618.

ParedesR.G.MartinezI. (2001). Naloxone blocks place preference conditioning after paced mating in female rats. — Behav. Neurosci. 115: 1363-1367.

PedersenA.TomaszyckiM.L. (2012). Oxytocin antagonist treatments alter the formation of pair relationships in zebra finches of both sexes. — Horm. Behav. 62: 113-119.

PfausJ.KippinT.Coria-AvilaG.GelezH.AfonsoV.IsmailN.ParadaM. (2012). Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance. — Arch. Sex. Behav. 41: 31-62.

ResendezS.L.KuhnmuenchM.KrzywosinskiT.AragonaB.J. (2012). κ-Opioid receptors within the nucleus accumbens shell mediate pair bond maintenance. — J. Neurosci. 32: 6771-6784.

RitersL.V. (2012). The role of motivation and reward neural systems in vocal communication in songbirds. — Front. Neuroendocrinol. 33: 194-209.

RitersL.V.AbsilP.BalthazartJ. (1999). Effects of naloxone on the acquisition and expression of appetitive and consummatory sexual behavior in male Japanese quail. — Physiol. Behav. 66: 763-773.

RitersL.V.EllisJ.M.AngyalC.S.BorkowskiV.J.CordesM.A.StevensonS.A. (2013). Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris). — Behav. Brain Res. 247: 117-124.

RitersL.V.SchroederM.B.AugerC.J.EensM.PinxtenR.BallG.F. (2005). Evidence for opioid involvement in the regulation of song production in male European starlings (Sturnus vulgaris). — Behav. Neurosci. 119: 245-255.

SchroederM.B.RitersL.V. (2006). Pharmacological manipulations of dopamine and opioids have differential effects on sexually motivated song in male European starlings. — Physiol. Behav. 88: 575-584.

ShayitM.NowakR.KellerM.WellerA. (2003). Establishment of a preference by the newborn lamb for its mother: the role of opioids. — Behav. Neurosci. 117: 446-454.

SilcoxA.P.EvansS.M. (1982). Factors affecting the formation and maintenance of pair bonds in the zebra finch, Taeniopygia guttata. — Anim. Behav. 30: 1237-1243.

SmileyK.O.VahabaD.M.TomaszyckiM.L. (2012). Behavioral effects of progesterone on pair bonding and partner preference in the female zebra finch (Taeniopygia guttata). — Behav. Proc. 90: 210-216.

TomaszyckiM.Adkins-ReganE. (2005). Experimental alteration of male song quality and output affects female mate choice and pair bond formation in zebra finches. — Anim. Behav. 70: 785-794.

VahabaD.M.LaceyW.H.TomaszyckiM.L. (2013). DSP-4, a noradrenergic neurotoxin, produces sex-specific effects on pairing and courtship behavior in zebra finches. — Behav. Brain Res. 252: 164-175.

WarnickJ.E.McCurdyC.R.SufkaK.J. (2005). Opioid receptor function in social attachment in young domestic fowl. — Behav. Brain Res. 160: 277-285.

Figures

  • The effects of 3 different doses of naloxone on directed and undirected singing in male zebra finches tested in a repeated measures design. Significant difference, p<0.05.

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  • The effects of 3 different doses of naloxone on directed singing to a familiar and an unfamiliar female in male zebra finches tested in a repeated measures design. Significant difference, p<0.05.

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  • The effects of 3 different doses of naloxone on male partner preferences in a forced-choice paradigm. Significant difference from chance, p<0.05.

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  • The effects of naloxone treatment on female partner preferences in a forced-choice paradigm. Each female was tested twice, and effects did not differ between tests, so each test was considered a separate data point. Significant difference from chance, p<0.05.

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  • The effects of naloxone treatment on clumping behaviour in female and male zebra finches. Significant difference, p<0.05.

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