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Conditioned Behaviour Mediated by Separate Nuclei Within Amygdala letters to nature only individuals descended from field-collected b-males, and then affect only two Ams genotypes: Tfr1Tfr2 females bearing b-alleles were assumed to a a mature as b-males, and Tfr1Tfr2, Ams Ams males were assumed to mature as Different types of fear- females. This latter effect assumed that the Tfr2 allele interacts with ECF, which b initially occurred only in parental -males, but which was transmitted to F1-2 conditioned behaviour individuals of both sexes and a range of Ams genotypes (Table 3b). Testing the model. In Tables 3a,b, exact probabilities were Bonferroni- mediated by separate adjusted (0.05/k, where k is the number of tests) when multiple crosses with identical Ams and Tfr genotypes, as well as ECF states were tested; similar nuclei within amygdala crosses with nonsignificant exact probabilities were pooled and the exact x2 probability for the pooled frequencies reported; primary sex-determination Simon Killcross*, Trevor W. Robbins & Barry J. Everitt genotypes were unambiguously determined from Pgm genotype frequencies Department of Experimental Psychology, University of Cambridge, within families; the apparent Tfr genotypes among 36 parents (24 crosses) were Downing Street, Cambridge CB2 3EB, UK 15 Tfr1Tfr1,12Tfr1Tfr2 and 9 Tfr2Tfr2; expected genotypes calculated from ......................................................................................................................... inferred allele frequencies conform to Hardy–Weinberg expectations, exact x2 The amygdala has long been thought to be involved in emotional probability 0.21. behaviour1,2, and its role in anxiety and conditioned fear has been highlighted3,4. Individual amygdaloid nuclei have been shown to Received 21 January; accepted 24 April 1997. project to various cortical and subcortical regions implicated in 1. Lank, D. B., Smith, C. M., Hanotte, O., Burke, T. & Cooke, F. Genetic polymorphism for alternative 5–7 mating behaviour in lekking male ruff. Nature 378, 59–62 (1995). affective processing . Here we show that some of these nuclei 2. Gross, M. R. Alternative reproductive strategies and tactics; diversity within sexes. Trends Ecol. Evol. have separate roles in distinct mechanisms underlying condi- 11, 92–97 (1996). tioned fear responses. Rats with lesions of the central nucleus 3. Sinervo, B. & Lively, C. M. The rock–paper–scissors game and the evolution of alternative male strategies. Nature 380, 240–243 (1996). exhibited reduction in the suppression of behaviour elicited by a 4. Shuster, S. M. Alternative reproductive behaviors: Three discrete male morphs in Paracerceis sculpta, conditioned fear stimulus, but were simultaneously able to direct an intertidal isopod from the northern Gulf of California. J. Crust. Biol. 7, 318–327 (1987). 5. Shuster, S. M. The reproductive behaviour of a-, b-, and g-males in Paracerceis sculpta, a marine their actions to avoid further presentations of this aversive isopod crustacean. Behaviour 121, 231–258 (1992). stimulus. In contrast, animals with lesions of the basolateral 6. Shuster, S. M. Male alternative reproductive behaviors in a marine isopod crustacean (Paracerceis amygdala were unable to avoid the conditioned aversive stimulus sculpta): The use of genetic markers to measure differences in fertilization success among a-, b- and g- males. Evolution 34, 1683–1698 (1989). by their choice behaviour, but exhibited normal conditioned 7. Shuster, S. M. & Wade, M. J. Equal mating success among male reproductive strategies in a marine suppression to this stimulus. This double dissociation demon- isopod. Nature 350, 606–61 (1991). 8. Sassaman, C. Inbreeding and sex ratio variation in female-biased populations of a clam shrimp, strates that distinct neural systems involving separate amygdaloid Eulimnadia texana. Bull. Mar. Sci. 45, 425–432 (1989). nuclei mediate different types of conditioned fear behaviour. We 9. Hartl, R. & Clark, A. in Principles of Population Genetics 2nd edn, 47–57 (Sinauer, Sunderland, MA, suggest that theories of amygdala function should take into 1989). 10. Heath, D. J. & Ratford, J. R. The inheritance of sex ratio in the isopod, Sphaeroma rugicauda. Heredity account the roles of discrete amygdala subsystems in controlling 64, 419–425 (1990). different components of integrated emotional responses. 11. Bull, J. J. Evolution of Sex Determining Mechanisms (Benjamin-Cummings, Menlo Park, CA, 1983). 12. Legrand, J. J., Legrand-Hamelin, E. & Juchault, P. Sex determination in Crustacea. Biol. Rev. 62, 439– Investigations of the neural basis of pavlovian fear conditioning 470 (1987). and its role in anxiety have suggested that the lateral nucleus of the 13. Juchault, P., Rigaud, T. & Mocquard, J.-P. Evolution of sex-determining mechanisms in a wild amygdala is the site of convergence of neural pathways that carry population of Armadillidium vulgare Latr. (Crustacea: Isopoda): competition between two feminizing parasitic sex factors. Heredity 69, 382–390 (1992). information about conditioned stimuli (CSs) and aversive rein- 14. Rousset, F., Bouchon, D., Pintureau, B., Juchault, P. & Solignac, M. Wolbachia endosymbionts forcers (USs)4,6. The emotional expression of this learned associa- responsible for various alterations of sexuality in Arthropods. Proc. R. Soc. Lond. B 250, 91–98 (1991). 15. Hurst, L. D. The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. tion may then be mediated by neural connections from the lateral to 4 Biol. Rev. 68, 121–193 (1993). the central nucleus of the amygdala , which, through its projections 16. Rigaud, T. & Juchault, P. Conflict between feminizing sex ratio distorters and an autosomal to hypothalamic and brainstem areas, is thereby able to coordinate masculinizing gene in the terrestrial isopod, Armadillidium vulgare Latr. Genetics 133, 247–252 (1993). the behavioural, endocrine and autonomic responses that form an 17. Juchault, P. & Rigaud, T. Evidence for female heterogamety in two terrestrial crustaceans and the integrated emotional response8. problem of sex chromosome evolution in isopods. Heredity 75, 488–471 (1995). 18. Read, T. R. C. & Cressie, N. A. C. in Goodness-of-fit Statistics for Discrete Multivariate Data 136–139 Serial processing in these regions of the amygdala is known to be (Springer, New York, 1988). involved in the acquisition and expression of conditioned fear 19. Shuster, S. M. & Wade, M. J. Female copying and sexual selection in a marine isopod crustacean. Anim. responses to aversive CSs, such as freezing and fear-potentiated Behav. 42, 1071–1078 (1991). 3–6 20. Shuster, S. M. in Crustacean Sexual Biology (eds Bauer, R. T. & Martin, J. W.) 91–110 (Columbia Univ. startle in animals . However, the role of these regions in alternative Press, New York, 1991). indices of fear conditioning, including the instrumental choice 21. Levins, R. Evolution in Changing Environments (Princeton Univ. Press, Princeton, 1968). 22. Slatkin, M. On the equilibration of fitnesses by natural selection. Am. Nat. 112, 845–859 (1978). responses involved in avoidance or conflict behaviour, is much 9 23. Maynard Smith, J. Evolution and the Theory of Games (Cambridge Univ. Press, New York, 1982). less clear . We therefore wished to investigate whether all forms of 24. Lively, C. M. Canalization versus developmental conversion in a spatially variable environment. Am. fear conditioning are mediated by this serial information flow Nat. 128, 561–572 (1986). 25. Slatkin, M. The evolutionary response to frequency and density dependent interactions. Am. Nat. 114, between the lateral and basal nuclei to the central nucleus of the 384–398 (1979). amygdala. To achieve this we designed a fear-conditioning proce- 26. Wright, S. Evolution and Genetics of Populations Vol. 2 (Univ. of Chicago Press 1969). 27. Wade, M. J., Shuster, S. M. & Stevens, L. Bottlenecks, founder events and inbreeding: Experimental dure in rats in which the development of an aversive CS–US studies of the response to selection with Tribolium. Evolution 50, 723–733 (1996). association could be assessed simultaneously by examination of 28. Shuster, S. M. Changes in female anatomy associated with the reproductive molt in Paracerceis sculpta two dissociable fear responses in the same animal. The aversive CS– (Holmes), a semelparous isopod crustacean. J. Zool. 225, 365–379 (1991). 29. Shuster, S. M. Courtship and female mate selection in a semelparous isopod crustacean (Paracerceis US association created by this procedure would not only produce a sculpta). Anim. Behav. 40, 390–399 (1990). pavlovian conditioned fear response, but would also provide the 30. Tinturier-Hamelin, E. Sur le polychromatisme de l’isopode Flabellifere Dynamene bidentata (Adams) II. Etude genetique du mutant bimaculata partiellement. Cah. Biol. Mar. 4, 473–591 (1967). necessary information for animals to solve an operant discrimina- tion that would lead to the avoidance of future presentations of the Acknowledgements. This research was supported by the NSF and by organized research and depart- aversive stimulus. mental funding from Northern Arizona University, and was authorized by the Mexican Government. We thank M. Wade and B. Charlesworth for reviewing data and earlier drafts of the manuscript; Y. Toquenaga Rats were trained on a concurrent conditioned-suppression and for statistical advice and for a program for calculating exact x2 tests; D. Dorado, S. Juarez, S. Hag, H. conditioned-punishment task (see Methods). Pressing one lever in Baitoo, S. Bhakta, Y. Bhakta, S. Brekhus;
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