appetitive behaviour; hippocampus; nucleus taeniae of the amygdalu; rhythmic cloacal sphincter movements; sexual conditioning
Abstract :
[en] We investigated the effects of presenting a sexual conditioned stimulus on the expression of c-fos in male Japanese quail. Eight brain sites were selected for analysis based on previous reports of c-fos expression in these areas correlated with sexual behaviour or learning. Males received either paired or explicitly unpaired presentations of an arbitrary stimulus and visual access to a female. Nine conditioning trials were conducted, one per day, for each subject. On the day following the ninth trial, subjects were exposed to the conditional stimulus (CS) for 5 min. Conditioning was confirmed by analysis of rhythmic cloacal sphincter movements (RCSM), an appetitive sexual behaviour, made in response to the CS presentation. Subjects in the paired condition performed significantly more RCSM than subjects in the unpaired group. Brains were collected 90 min following the stimulus exposure and stained by immunolhistochemistry for the FOS protein. Significant group differences in the number of FOS-immunoreactive (FOS-ir) cells were found in two brain regions, the nucleus taeniae of the amygdala (TnA) and the hippocampus (Hp). Subjects in the paired condition had fewer FOS-ir cells in both areas than subjects in the unpaired condition. These data provide additional support to the hypothesis that TnA is implicated in the expression of appetitive sexual behaviours in male quail and corroborate numerous previous reports of the involvement of the hippocampus in conditioning. Further, these data suggest that conditioned and unconditioned sexual stimuli activate different brain regions but have similar behavioural consequences.
Disciplines :
Neurosciences & behavior
Author, co-author :
Taziaux, Mélanie ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Lopez, J.
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Holloway, K. S.
Language :
English
Title :
Differential c-fos expression in the brain of male Japanese quail following exposure to stimuli that predict or do not predict the arrival of a female
Abercrombie, M. (1946) Estimation of nuclear population from microtome sections. Anat. Rec., 94, 239 247.
Absil, P., Braquenier, J.B. Balthazart, J. (2002) Effects of lesions of nucleus taeniae on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Brain Behav. Evol., 60, 13 35.
Adkins-Regan, E. (1999) Foam produced by the male Coturnix quail: What is its function? Auk, 116, 184 193.
Adkins-Regan, E. MacKillop, E.A. (2003) Japanese quail (Coturnix japonica) inseminations are more likely to fertilize eggs in a context predicting mating opportunities. Proc. R. Soc. London, 270, 1685 1689.
Aste, N., Balthazart, J., Absil, P., Grossmann, R., Mülhbauer, E., Viglietti-Panzica, C. Panzica, G.C. (1998) Anatomical and neurochemical definition of the nucleus of the stria terminalis in Japanese quail (Coturnix japonica). J. Comp. Neurol., 396, 141 157.
Atoji, Y. Wild, J.M. (2006) Anatomy of the avian hippocampal formation. Rev. Neurosci., 17, 3 15.
Atoji, Y., Wild, J.M., Yamamoto, Y. Suzuki, Y. (2002) Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J. Comp. Neurol., 447, 177 199.
Balthazart, J., Absil, P., Gerard, M., Appeltants, D. Ball, G.F. (1998) Appetitive and consummatory male sexual behavior in japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J. Neurosci., 18, 6512 6527.
Baum, M.J. Everitt, B.J. (1992) Increased expression of c-fos in the medial preoptic area after mating in male rats: Role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience, 50, 627 646.
Baylé, J.D., Ramade, F. Oliver, J. (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J. Physiol. (Paris), 68, 219 241.
Beach, F.A. (1956) Characteristics of masculine 'sex drive'. Nebraska Symp. Motivation, 4, 1 32.
Beck, C.H. Fibiger, H.C. (1995) Conditioned fear-induced changes in behavior and in the expression of immediate early gene c-fos: With and without diazepam pretreatment. J. Neurosci., 15, 709 720.
Bertaina-Anglade, V., Tramu, G. Destrade, C. (2000) Differential learning-stage dependent patterns of c-Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. Eur. J. Neurosci., 12, 3803 3812.
Bingman, V.P., Ioale, P., Casini, G. Bagnoli, P. (1990) The avian hippocampus: evidence for a role in the development of the homing pigeon navigational map. Behav. Neurosci., 104, 906 911.
Brito, I., Britto, L.R.G. Ferrari, E.A.M. (2006) Classical tone-shock conditioning induces zenk expression in the pigeon (Columba livia) hippocampus. Behav. Neurosci., 120, 353 361.
Charlier, T.D., Ball, G.F. Balthazart, J. (2005) Sexual behavior activates the expression of the immediate early genes c-fos and zenk (EGR-1) in catacholaminergic neurons of male Japanese quail. Neuroscience, 131, 13 30.
Cheng, K.M., Hickman, A.R. Nichols, C.R. (1989a) Role of the proctodeal gland foam of male Japanese quail in natural copulations. Auk, 106, 279 285.
Coolen, L.M., Peters, H.J.P.W. Veening, J.G. (1996) Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res., 738, 67 82.
D'Hondt, E., Vermeiren, J., Peeters, K., Balthazart, J., Tlemçani, O., Ball, G.F., Duffy, D.L., Vandesande, F. Berghman, L.R. (1999) Validation of a new antiserum directed towards the synthetic c-terminus of the FOS protein in avian species: Immunological, physiological and behavioral evidence. J. Neurosci. Meth., 91, 31 45.
Delville, Y., Sulon, J. Balthazart, J. (1986) Diurnal variations of sexual receptivity in the female Japanese quail (Coturnix coturnix japonica). Horm. Behav., 20, 13 33.
Domjan, M., Blesbois, E. Williams, J. (1998) The adaptive significance of sexual conditioning: Pavlovian control of sperm release. Psychol. Sci., 9, 411 415.
Fernandez-Fewell, G.D. Meredith, M. (1994) c-fos expression in vomeronasal pathways of mated or pheremone-stimulated male golden hamsters: Contributions from vomeronasal sensory input and expression related to mating performance. J. Neurosci., 14, 3643 3654.
Fujiwara, K.T., Ashida, K., Nishima, H., Iba, H., Miyajima, N., Nishizawa, M. Kawai, S. (1987) The chicken c-fos gene: Cloning and nucleotide sequence analysis. J. Virol., 61, 4012 4018.
Gagliardo, A., Ioale, P. Bingman, V.P. (1999) Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. J. Neurosci., 19, 311 315.
Gall, C.M., Hess, U.S. Lynch, G. (1998) Mapping brain networks engaged by, and changed by, learning. Neurobiol. Learning Memory, 70, 14 36.
Giantonio, G.W., Lund, N.L. Gerall, A.A. (1970) Effect of diencephalic and rhinencephalic lesions on the male rat's sexual behavior. J. Comp. Physiol. Psychol., 73, 38 46.
Gutierrez, G. Domjan, M. (1996) Learning and male-male sexual competition in Japanese quail (Coturnix coturnix japonica). J. Comp. Psychol., 110, 170 175.
Hall, J., Thomas, K.L. Everitt, B.J. (2001) Fear memory retrieval induces CREB phosphorylation and Fos expression within the amygdala. Eur. J. Neurosci., 13, 1453 1458.
Hampton, R.R. Shettleworth, S.J. (1996) Hippocampal lesions impair memory formation for location but not color in passerine birds. Behav. Neurosci., 110, 831 835.
Harris, V.S. Sachs, B.D. (1975) Copulatory behavior in male rats following amygdaloid lesions. Brain Res., 86, 514 518.
He, J., Yamada, K. Nabeshima, T. (2002) A role of Fos expression in the CA3 region of the hippocampus in spatial memory formation in rats. Neuropsychopharmacology, 26, 259 268.
Heeb, M.M. Yahr, P. (1996) c-fos immunoreactivity in the sexually dimorphic area of the hypothalamus and related brain regions of male gerbils after exposure to sex-related stimuli or performance of specific sexual behaviors. Neuroscience, 72, 1049 1071.
Hess, U.S., Gall, C.M., Granger, R. Lynch, G. (1997) Differential patterns of c-fos mRNA expression in amygdala during successive stages of odor discrimination learning. Learning Memory, 4, 262 283.
Holland, P.C. Rescorla, R.A. (1975) The effects of two ways of devaluing the unconditioned stimulus after first- and second-order appetitive conditioning. J. Exp. Psychol. Anim. Behav. Proc., 1, 355 363.
Holland, P.C. Straub, J.J. (1979) Differential effects of two ways of devaluing the unconditioned stimulus after Pavlovian appetitive conditioning. J. Exp. Psychol. Anim. Behav. Proc., 1, 65 78.
Hollis, K.L., Pharr, V.L., Dumas, M.J., Britton, G.B. Field, J. (1997) Classical conditioning provides paternity advantage for territorial blue gouramies (Trichogaster trichopterus). J. Comp. Psychol., 111, 219 225.
Holloway, K.S., Balthazart, J. Cornil, C.A. (2005) Androgen mediation of conditioned rhythmic cloacal sphincter movements in Japanese quail. J. Comp. Psychol., 119, 49 57.
Holloway, K.S. Domjan, M. (1993) Sexual approach conditioning: Tests of unconditioned stimulus devaluation using hormone manipulations. J. Exp. Psychol. Anim. Behav. Proc., 19, 47 55.
Irwin, K.B., Craig, A.D., Bracha, V. Bloedel, J.R. (1992) Distribution of c-fos expression in brainstem neurons associated with conditioning and pseudo-conditioning of the rabbit nictitating membrane reflex. Neurosci. Ltrs., 148, 71 75.
de Jonge, F.H., Oldenburger, W.P., Louwerse, A.L. Van de Poll, N.E. (1992) Changes in male copulatory behavior after sexual exciting stimuli: Effects of medial amygdala lesions. Physiol. Behav., 52, 327 332.
Kelly, M.P. Deadwyler, S.A. (2002) Acquisition of a novel behavior induces higher levels of ARC mRNA than does overtrained performance. Neuroscience, 110, 617 626.
Kippin, T.E., Cain, S.W. Pfaus, J.G. (2003) Estrous odors and sexually conditioned neutral odors activate separate neural pathways in the male rat. Neuroscience, 117, 971 979.
Kondo, Y. (1992) Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiol. Behav., 51, 939 943.
Kuenzel, W.J. Masson, M. (1988) A Stereotaxic Atlas of the Brain of the Chick (Gallus Domesticus). The Johns Hopkins University Press, Baltimore.
Meddle, S.L., King, V.M., Follett, B.K., Wingfield, J.C., Ramenofsky, M., Foidart, A. Balthazart, J. (1997) Copulation activates fos-like immunoreactivity in the male quail forebrain. Behav. Brain Res., 85, 143 159.
Newman, S.W., Parfitt, D.B. Kollack-Walker, S. (1997) Mating induced c-fos expression patterns complement and supplement observations after lesions in the male Syrian hamster brain. Ann. N.Y. Acad. Sci., 807, 239 259.
Nikolakopoulou, A.M., Davies, H.A. Stewart, M.G. (2006) Passive avoidance training decrease synapse density in the hippocampus of the domestic chick. Eur. J. Neurosci., 23, 1054 1062.
Nordquist, R.E., Pennartz, C.M.A., Uylings, H.B.M., Joosten, R.N.J.M.A., Jonker, A.J., Grouenewegen, H.J. Voorn, P. (2003) C-fos activation patterns in rat prefrontal cortex during acquisition of a cued classical conditioning task. Behav. Brain Res., 146, 65 75.
Panzica, G.C., Viglietti-Panzica, C. Balthazart, J. (1996) The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol., 17, 51 125.
Papa, M., Pellicano, M.P., Welzl, H. Sadile, A.G. (1993) Distributed changes in c-Fos and c-Jun immunoreactivity in the rat brain associated with arousal and habituation to novelty. Brain Res. Bull., 32, 509 515.
Pezzone, M.A., Lee, W.-S., Hoffman, G.E. Rabin, B.S. (1992) Induction of c-Fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res., 597, 41 50.
Pfaus, J.G. Heeb, M.M. (1997) Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res. Bull., 44, 397 407.
Radulovic, J., Kammermeier, J. Spiess, J. (1998) Relationship between Fos production and classical fear conditioning: Effects of novelty, latent inhibition, and unconditioned stimulus presentation. J. Neurosci., 18, 7452 7461.
Reiner, A.D., Perkel, J., Bruce, L., Butler, A., Csillag, A., Kuenzel, W., Medina, L., Paxinos, G., Shimizu, T., Striedter, G., Wild, M., Ball, G.F., Durand, S., Güntürkün, O., Lee, D.W., Mello, C.V., White, S.A., Hough, G., Kubikova, L., Smulders, T.V., Wada, K., Dugas-Ford, J., Husband, S., Yamamoto, K., Yu, J., Siang, C. Jarvis, E.D. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol., 473, 377 414.
Rosen, J.B., Fanselow, M.S., Young, S.L., Sitcoske, M. Maren, S. (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res., 796, 132 142.
Roullet, F., Datiche, F., Lienard, F. Cattarelli, M. (2005) Learning-stage dependent Fos expression in the rat brain during acquisition of an olfactory discrimination task. Behav. Brain Res., 157, 127 137.
Seiwert, C.M. Adkins-Regan, E. (1998) The foam production system of the male Japanese quail: Characterization of structure and function. Brain Behav. Evol., 52, 61 80.
Shimizu, T., Bowers, A.N., Budzynski, C.A., Kahn, M.C. Bingman, V.P. (2004) What does a pigeon (Columba livia) brain look like during homing? Selective examination of ZENK expression. Behav. Neurosci., 118, 845 851.
Silberberg, A. Adler, N. (1974) Modulation of the copulatory sequence of the male rat by a schedule of reinforcement. Science, 185, 374 376.
Smulders, T.V. DeVoogd, T.J. (2000) Expression of immediate early genes in the hippocampal formation of the black-capped chickadee (Poecile atricapillus) during a food hoarding task. Behav. Brain Res., 114, 39 49.
Taziaux, M., Cornil, C.A., Dejace, C., Arckens, L., Ball, G.F. Balthazart, J. (2006) Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur. J. Neurosci., 23, 1869 1887.
Thompson, R.R., Goodson, J.L., Ruscio, M.G. Adkins-Regan, E. (1998) Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals. Brain Behav. Evol., 51, 215 229.
Tlemçani, O., Ball, G.F., D'Hondt, E., Vandesande, F., Sharp, P.J. Balthazart, J. (2000) Fos induction in the Japanese quail brain after expression of appetitive and consummatory aspects of male sexual behavior. Brain Res. Bull., 52, 249 262.
Unal, B., Bradley, P.M., Sahin, B., Canan, S., Aslan, H. Kaplan, S. (2002) Estimation of numerical density and mean synaptic height in chick hippocampus 24 and 48 hours after passive avoidance training. Brain Res. Dev. Brain Res., 136, 135 144.
Veening, J.G. Coolen, L.M. (1998) Neural activation following sexual behavior in the male and female rat brain. Behav. Brain Res., 92, 181 193.
Wilson, W.O. Huang, R.H. (1962) A comparison of the time of ovipositing for Coturnix and chicken. Poultry Sci., 41, 1843 1845.
Wood, R.I. Newman, S.W. (1995) Hormonal influence on neurons of the mating behavior pathway in male hamsters. In Micevych, P.E. Hammer, R.P.J., (Eds), Neurobiological Effects of Sex Steroid Hormones. Cambridge University Press, Cambridge, UK, pp. 3 39.
Wood, R.I. Swann, J.M. (2000) Neuronal integration of chemosensory and hormonal signals in the control of male sexual behavior. In Wallen, K. Schneider, J.E., (Eds), Reproduction in Context. MIT Press, Cambridge, MA, pp. 423 444.
Zamble, E., Hadad, M., Mitchell, J.B. Cutmore, T.R.H. (1985) Pavlovian conditioning of sexual arousal: First- and second-order effects. J. Exp. Psychol. Anim. Behav. Proc., 11, 598 610.