Hormones and Behavior 49 (2006) 577 – 579 www.elsevier.com/locate/yhbeh

Commentary

Relationships among hormones, brain and behavior: Exceptions in search of a rule? Juli Wade ⁎ Michigan State University, Departments of Psychology and Zoology and Neuroscience Program, 108 Giltner Hall, East Lansing, MI 48824-1101, USA Received 31 December 2005; revised 19 January 2006; accepted 19 January 2006 Available online 28 February 2006

Relationships among hormones, brain and behavior have intrigued researchers for many years. A wealth of literature has accumulated in this field since publication of the landmark paper by Phoenix et al. (1959) that documented early “organizational” and adult “activational” effects of steroid hormones on the display of masculine sexual behaviors in the guinea pig. While that paper did not directly investigate the brain, it set the stage, ending with: “An assumption seldom made explicit is that modification of behavior follows an alteration in the structure or function of the neural correlates of the behavior. We are assuming that testosterone or some metabolite acts on those central nervous tissues in which patterns of sexual behavior are organized….” The earliest reports of sex differences in brain morphology and their hormonal regulation (e.g., Dörner and Staudt, 1968, 1969; Pfaff, 1966; Raisman and Field, 1971) focused on quite small structures—cell nuclei, nucleoli, and synapses. Then, Nottebohm and Arnold (1976) reported substantial sex differences in the volume of brain areas with known functions. Regions of the forebrain that control masculine singing behavior are approximately 3- to 5-fold larger in volume in males than females. This original report on songbirds was done in zebra finches and canaries, but a variety of investigators have since extended it to numerous avian species, documenting relationships between morphology and behavior, as well as uncovering hormonal and other mechanisms facilitating structural and functional change (reviewed in various chapters in Zeigler and Marler, 2004). Over the last 40 years, this type of work has been expanded to include other forebrain and neuromuscular systems involved in the control of reproductive ⁎ Fax: +1 517 432 2744. E-mail address: [email protected] 0018-506X/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2006.01.004

behaviors in representatives of diverse vertebrate groups (see reviews in Cooke et al., 1998; Crews and Moore, 2005; Pfaff et al., 2002; Wade, 2005). Parallels between morphology and function, as well as roles for testosterone in development and seasonal changes in adulthood, have been broadly identified. However, inconsistencies have accumulated. For example, several dissociations exist among testosterone concentrations, the size of song control nuclei and singing behavior, particularly from field-caught birds (Ball et al., 2004, although see Garamszegi and Eens, 2004). In whiptails lizards, adult testosterone increases masculine sexual behaviors in both sexes, but only induces changes in the volume of limbic brain regions in males (Wade et al., 1993). And, in rodents, negative correlations between copulatory behavior and motoneuron soma size have been reported (Breedlove, 1997, but see Raouf et al., 2000). The very interesting paper by Kabelik et al. (2006) in the present issue extends these types of results, providing novel information on a number of levels. This heroic study concerns relationships among hormones, limbic brain nuclei and aggressive behaviors, which nicely complements the research that has more commonly investigated morphological parallels with degree of sexual function (Simerly, 2002; also see above). It utilizes a unique, reptilian species including two morphs of males with alternative reproductive strategies, one of which is more aggressive and territorial than the other. This model therefore offers the potential to investigate not only differences between the sexes, but also between groups of males that typically behave quite differently (similar to elegant work in fish; Grober and Bass, 2002). The authors examined circulating hormone levels and volumes of the lateral septum, preoptic area, amygdala and ventromedial hypothalamus across seasons and reproductive states following staged territorial intrusions in the

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J. Wade / Hormones and Behavior 49 (2006) 577–579

field. Thus, like other studies on wild individuals, this work offers the substantial advantage of analyzing the relationships among hormones, brain and behavior in a natural, unmanipulated population. Of course, this strategy also has its pitfalls, including fluctuating steroid levels (compared to those provided by implants) and an unexpected lack of a difference in aggression levels between the two male morphs. Thus, as is common in these types of studies, the very features that are strengths also present some limitations for interpretation. Nonetheless, the intriguing study by Kabelik et al. (2006) provides some striking examples of dissociations among the size of brain regions, behavioral output and plasma hormone concentrations. Interestingly, both sex and seasonal differences in the volumes of limbic brain nuclei were detected, but the brain regions were equivalent among groups of males with different frequencies and/or intensities of aggressive behaviors and among males with partially regressed vs. fully developed testes. Increased plasma testosterone was associated with aggressive displays, yet the level of behavior did not differ with breeding season or reproductive state. Also, seasonal changes in brain nucleus volumes were observed in females, but their reproductive states did not predict this neural plasticity. Collectively, these results suggest that larger volumes of the evaluated brain regions are not required for the display of these behaviors, and conversely, that increased behavioral function does not necessarily enlarge particular brain regions. In addition, the present study is consistent with some others showing that adult testosterone does not always increase the size of sexually dimorphic brain regions and that other factors contribute to seasonal changes in brain region volume (Ball et al., 2004). Clear parallels among levels of gonadal hormones, brain morphology and behavior are somehow comforting, but as exceptions such as those documented by Kabelik et al. (2006) continue to be revealed, it is worth asking whether patterns exist among them. A variety of factors might be considered. Does it matter whether behavior was assessed and/or tissue collected in the lab or the field, and if so, why? For example, is variability in results between these settings due to technical factors or to a set of identifiable features of the social or abiotic environment that induces specific physiological changes in the animals? Similarly, are differences between species in the nature of correlations among hormone levels, neural structure and behavior due to distinct ecological factors, and if so, which ones? The specific aspects of behavior could also influence the results, for example whether one is investigating courtship, copulation or territorial aggression. All may be required for successful reproduction and tend to be influenced by testosterone in males, yet they are discrete functions. Similarly, do consistent differences exist in the responses of regions of the nervous system more involved with motivation, as in the present study, compared to motor nuclei that are more directly involved with the mechanics of behavioral production? Even considering these issues, it may for a while be difficult to draw firm conclusions for several reasons. For example, in many studies only one or a few relatively gross anatomical

features are quantified. The more brain regions and the smaller the unit of analysis, such as number of neurons or characteristics of individual cells (e.g., the number of dendritic spines), the easier it is to hypothesize about potential relationships to function (both of the previous examples would allow for increased communication between cells or brain regions). Measuring volume may be a good first pass at what could be a very time-consuming analysis—if a difference in volume is not detected, it is possible that differences in features such as neuron size, number or arborization do not exist or are not large enough to be biologically relevant. However, that may not necessarily be the case, as they could offset each other. Another factor regarding analysis involves whether mean differences are compared across groups rather than, or in addition to, direct correlations among morphology, behavioral function and hormone levels. Certainly, important relationships should be reflected in large group differences, but one might also expect enhanced morphology to be directly associated with increased function within groups of individuals. The nature of assessment of hormone levels should also be considered. Presumably, if one wants to determine their effects on brain structure or function, then levels in the brain are more relevant than those circulating in plasma. It would be extremely difficult if not impossible, however, to assay hormone concentrations in the same brain regions of the same individuals in which morphology was analyzed. Related to this point, as Kabelik et al. (2006) note, hormones assayed from plasma reflect point measures and may not be indicative of levels over the entire period of time required to sculpt morphological changes in the nervous system or even to prime behaviors. To complicate matters even further, in some cases the specific function of particular brain regions is not well delineated or the area is involved in more than one function; this is particularly true for limbic regions. Furthermore, even when a distinct role of a neural structure in behavioral regulation is identified along with a correlation between morphology and level of function, a causal relationship does not necessarily exist or its direction is not clear. One can begin to address this issue by independently manipulating behavior and assessing the effect on morphology. However, the reverse, manipulating the size of neural structures to test direct effects on function, is extremely difficult if not impossible. Given these sorts of issues, do we have any hope of uncovering principles guiding morphological and behavioral change in the adult nervous system? Absolutely! Investigating the relationships broadly, under multiple conditions across diverse species, and synthesizing the results with awareness of their limitations will provide insights leading to that goal. It is these challenges and the cases which do not so neatly fit the dogma that high testosterone, larger brain regions and behavior all go hand in hand (in hand) that make this work exciting. Acknowledgments JW is funded by the NIH (R01-MH55488 and K02MH065907) and the NSF (IBN-0234740). Thanks to Joe Lonstein and David Crews for thoughtful comments on the manuscript.

J. Wade / Hormones and Behavior 49 (2006) 577–579

References Ball, G.F., Auger, C.J., Bernard, D.J., Charlier, T.D., Sartor, J.J., Riters, L.V., Balthazart, J., 2004. Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. In: Zeigler, H.P., Marler, P. (Eds.), Behavioral Neurobiology of Birdsong. Ann. NY Acad. Sci., New York, pp. 586–610. Breedlove, S.M., 1997. Sex on the brain. Nature 389, 801. Cooke, B., Hegstrom, C.D., Villeneuve, L.S., Breedlove, S.M., 1998. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol. 19, 323–362. Crews, D., Moore, M.C., 2005. Historical contributions of research on reptiles to behavioral neuroendocrinology. Horm. Behav. 48, 384–394. Dörner, G., Staudt, J.S., 1968. Structural changes in the preoptic anterior hypothalamic area of the male rat, following neonatal castration and androgen substitution. Neuroendocrinology 3, 136–140. Dörner, G., Staudt, J.S., 1969. Structural changes in the hypothalamic ventromedial nucleus of the male rat, following neonatal castration and androgen treatment. Neuroendocrinology 4, 278–281. Garamszegi, L.Z., Eens, M., 2004. Brain space for a learned task: strong intraspecific evidence of neural correlates of singing behavior in songbirds. Brain Res. Rev. 44, 187–193. Grober, M.S., Bass, A.H., 2002. Life history, neuroendocrinology, and behavior in fish. In: Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E., Rubin, R.T. (Eds.), Hormones, Brain and Behavior. Academic Press, New York, pp. 331–347. Kabelik, D., Weiss, S.L., Moore, M.C., 2006. Steroid hormone mediation of

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limbic brain plasticity and aggression in free-living tree lizards, Urosaurus ornatus. Horm. Behav. 49, 587–597 doi:10.1016/j.yhbeh.2005.12.004. Nottebohm, F., Arnold, A.P., 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194, 211–213. Pfaff, D.W., 1966. Morphological changes in the brains of adult male rats after neonatal castration. J. Endocrinol. 36, 415–416. Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E., Rubin, R.T. (Eds.), 2002. Hormones, Brain and Behavior. Academic Press, New York. Phoenix, C.H., Goy, R.W., Gerall, A.A., Young, W.C., 1959. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369–382. Raisman, G., Field, P.M., 1971. Sexual dimorphism in the preoptic area of the rat. Science 173, 731–733. Raouf, S., Van Roo, B., Sengelaub, D., 2000. Adult plasticity in hormonesensitive motoneuron morphology: methodological/behavioral confounds. Horm. Behav. 38, 210–221. Simerly, R.B., 2002. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25, 507–536. Wade, J., 2005. Current research on the behavioral neuroendocrinology of reptiles. Horm. Behav. 48, 451–460. Wade, J., Huang, J.-M., Crews, D., 1993. Hormonal control of sex differences in the brain, behavior and accessory sex structures of whiptail lizards (Cnemidophorus species). J. Neuroendocrinol. 5, 81–93. Zeigler, H.P., Marler, P. (Eds.), 2004. Behavioral Neurobiology of Birdsong, vol. 1016. New York Academy of Sciences, New York.

Relationships among hormones, brain and behavior

Raouf, S., Van Roo, B., Sengelaub, D., 2000. Adult plasticity in hormone- sensitive motoneuron morphology: methodological/behavioral confounds. Horm. Behav ...

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