By Donna L. Maney, PhD
Hormones Excite the Senses
Behavioral endocrinologists are fond of saying that hormones don't cause behavior. This tenet dates back to the father of behavioral endocrinology himself, Frank Beach (1948), who noted that even when an animal's levels of reproductive hormones are high, social behavior is limited to specific contexts and therefore won't occur in the absence of appropriate external sensory cues. Beach argued that these sensory cues, which could take the form of courtship displays, aggressive threats, or crying babies, may act as triggers for behavioral responses, whereas hormones raise and lower the threshold for performing those responses. In other words, when you encounter that crying baby or the "How YOO doin'?" from that guy in the bar, your behavioral response may depend on your hormones--but without that visual or auditory (or perhaps olfactory) signal, you aren't likely to perform that response at all.
In the above scenario, sensory and hormonal inputs arrive through different doors at the same hypothetical spot in the brain, usually called a "motivational center." At that point their influences sum and, if the total stimulation is above threshold, the message is sent to motor systems that a behavior needs to happen. The idea that the sensory and hormonal influences meet for the first time in the motivational center has, however, been quietly poo-pooed for decades. Beach himself argued that hormones affect the periphery and thus the sensations that are perceived. Over the last fifty years, many investigators have shown that hormones can have profound effects on sensory systems themselves, to the extent that detection thresholds and discrimination ability can be altered. In both rats and humans, for example, the ability to detect odors is greater during periods of high estrogen than during other phases of the reproductive cycle, and estrogen treatment improves olfactory sensitivity in ovariectomized rats and postmenopausal women (Caruso et al., 2001; Caruso et al., 2004; Pietras & Moulton, 1974). Hormones, particularly gonadal steroids, may therefore affect not only our behavioral responses to sensory stimuli but whether we can tell one stimulus apart from others, or even detect it at all. Our hormones thus affect the way we perceive the world around us.
Of all the sensory stimuli available to us, perhaps none are more important than those associated with successful reproduction--such as the courtship signals of a potential mate. We might predict, then, that if reproductive hormones affect sensory transduction or processing in a given species, they are most likely to affect the modalities most important for communication of sociosexual signals in that species. In rodents, which have exquisitely developed pheromonal communication systems, receptors for both estrogens and androgens can be found in the olfactory bulb--most notably in cells that are known to help sharpen discrimination of similar odors (Kelliher et al., 1998; Yokoi et al., 1995). Within both the bulb and the olfactory epithelium, cellular responses to opposite-sex pheromonal stimulation are significantly greater in rodents treated with gonadal hormones than in their gonadectomized counterparts (e.g., Halem et al., 1999). In the tropical fish known as the tinfoil barb, gonadal hormones dramatically increase the sensitivity of peripheral olfactory receptors to fish pheromones (Cardwell et al., 1995), thus enabling them to smell each other more easily when their levels of these hormones are high. In fish that have evolved auditory communication, preferring to hum to each other in addition to emitting the old-fashioned pheromones, the tuning of the female's inner ear depends on her levels of estrogen (Sisneros et al., 2004). During times when she is most fertile and estrogen is high, her ears are much more sensitive to the particular frequency at which the male hums, and she responds by swimming in his direction. After she has spent all her eggs and her estrogen levels drop, she doesn't give a whit about his humming and probably can't hear it as well as before, either (Sisneros & Bass, 2003).
Perhaps the most famous auditory courtship signal (other than our own "How YOO doin'") is the widely diverse and often seasonal subject of my own work, bird song. Both male and female songbirds sing for many reasons in many contexts, but in North America the males are doing most of the singing, and they do their courtship singing in the spring. In many species, the female will respond to the sexiest male songs by performing what's called a "copulation solicitation display," which is exactly what it sounds like. She raises her tail and head (see the bird in the figure), quivers her wings, and lets out a trill, all of which signals to the male that he's passed the test and she's ready to mate. The display is highly estrogen dependent, occurring only during the breeding season when estrogen levels are high. During the non-breeding season, when the females' estrogen levels are low, males still sing but of course it's not the right time of year to interpret that as a sexual advance. So the females politely pay attention to these winter songs, which are likely to signal defensive feelings, but do not respond by soliciting copulation outside the breeding season--doing so might be considered socially inappropriate and downright rude. The female's estrogen levels, which are tightly controlled by the time of year, make sure that the females respond with the display only when it's a reasonable thing to do.
In my lab, we are interested in finding out how hormones such as estrogen so dramatically change the female's behavioral response to male song. We take advantage of the fact that when treated with estrogen, laboratory-housed female White-throated Sparrows (Zonotrichia albicollis) will perform beautiful displays in response to audio recordings of male song. We can play them sexy songs, record their behavioral responses, and then use immunocytochemical techniques to look for something called a "genomic response"-- the expression of immediate early genes, which are transiently expressed in neurons undergoing sustained depolarization related to neuronal plasticity (see Mello et al., 2004). In other words, we can actually look in the auditory regions of the brain to see which neurons are responding to the song with increases in activity. We've known for some time now that the more behaviorally relevant the sound, the greater the genomic response in the auditory forebrain. Mello et al. (1992) showed that in canaries and zebra finches, hearing synthetic beeps induced only a small genomic response, whereas heterospecific song induced a somewhat larger response and conspecific song a much larger one. Since that study, many researchers have shown support for this general relation between the behavioral salience of the stimulus and the genomic response --for example, we've shown that more familiar, preferred songs induced a greater response than unfamiliar ones (Maney et al., 2003). All of these studies, however, were conducted on birds in breeding condition with plenty of reproductive hormones.
Recently, we compared estrogen-treated females with females that were not treated with hormones (Maney et al., 2006). Both groups of birds were otherwise in non-breeding condition. We played these females recordings of either male song or synthetic, frequency-matched beeps. As expected, in the estrogen-treated birds the genomic response to song was far greater than the response to beeps. In the untreated birds, however, the response was not selective for song. In other words, without breeding levels of estrogen, the genomic response to song was equal to the response to beeps. We saw this effect not only in the auditory forebrain, but also in the inferior colliculus, an auditory processing area upstream of the forebrain (see Figure). Interestingly, the response was just as high to both sorts of auditory stimuli in the untreated females as it was to song in the treated females. The main difference between estrogen-treated and untreated birds was not, therefore, that estrogen increased the response to song. Rather, estrogen decreased the response to beeps.
Foreground: A female White-crowned Sparrow (Zonotrichia leucophrys) performs a copulation solicitation display in response to a recording of male song. Background: Photomicrograph showing the song-induced genomic response in the inferior colliculus, an auditory processing area. The black dots represent cell nuclei immunoreactive for the protein product of the immediate early gene zenk, which is expressed in cells undergoing sustained depolarization.
Our results remind me of an over-arching principle in neuroscience--that sensory systems of all modalities are designed to dampen responses to non-relevant stimuli, particularly those near the perceptual "edges" of relevant stimuli. Such inhibition sharpens the contrast between auditory stimuli, and may aid in both detection and discrimination of those sounds that are particularly relevant. But what if the behavioral relevance of a signal changes over time-what if an individual needs to pay attention to a sound today that she could have disregarded yesterday? Decades of research have shown that the auditory system does a great job of keeping up with what is relevant and processing it accordingly. For example, when animals are trained to associate a reward or a punishment with specific sounds, those sounds become over-represented in the auditory cortex as neurons that previously responded best to other stimuli are co-opted to respond to new, behaviorally relevant ones (Bakin & Weinberger, 1990; Bao, et al., 2001; Recanzone et al., 1993). By learning which stimuli to pay attention to, and by inhibiting auditory responses to non-target stimuli, the brain ensures that the most important signals will be processed properly and given the attention they deserve. Whether hormones can enhance or even mimic the effects of learning is a future area of research.
What subjective experience results from enhanced auditory selectivity for song during the breeding season? When I think about this question, I am always reminded of the year or two I spent at the beginning of this decade watching home decorating shows on television. No matter which network, whether the decorating was being done by well--intentioned neighbors or The Fab Five, invariably there would come the point where the designer announces, "Now we're going to pop the couch!" For those unfamiliar with this exercise, it involves decorating an entire room completely in beige--wall, floor, furniture, etc-then upholstering the couch in lime green chenille.
The couch then "pops" visually against the bland background, and the lucky homeowner beams with gratitude. Perhaps to our listening female, estrogen "pops" male song such that in the breeding season her auditory system enhances the contrast between song and less relevant sounds. Then, after the breeding season is over, she can still hear and attend to song, but she's not listening for it the way she once was. Her auditory system responds similarly to other sounds, too, like strange, unexplained beeping noises.
Can hormones "pop" sociosexual signals in humans? The literature suggests that perhaps they can. Researchers conducting studies in humans, however, usually report effects on signal preference rather than detection or discrimination, leaving open the possibility that signal salience is actually unaffected by hormones. Such studies are nonetheless very interesting; for example, in studies of visual preference, ovulating women judged photos of darker and more masculine faces to be more attractive than women in other phases of their cycles (Frost, 1994; Penton-Voak et al., 1999). Ovulation is also associated with an auditory preference for deeper, more masculine voices (Feinberg et al., 2006; Puts, 2005). Surprisingly, some studies even suggest that ovulatory hormones may influence olfactory preferences in humans. Rikowski and Grammer (1999) asked men to sleep in cotton T-shirts for a couple of nights, then asked women to judge the attractiveness of the odors of those T-shirts. An independent group of women rated the visual attractiveness of the same men, using photographs. The ratings of the viewers and the sniffers were positively correlated, meaning that the visually attractive men also smelled more attractive. This correlation, however, was significant only in ovulating women. Women in other phases of their cycles found the visually appealing men to smell just as bad as the ugly men, meaning that the preference for the odors of attractive men may depend on ovulatory hormones. It's actually no surprise that olfactory systems may be sensitive to hormonal modulation, because pheromones that we presumably smell are themselves derivatives of steroid hormones. Pheromonal communication probably evolved as a way for us to judge the reproductive hormone level, and thus reproductive readiness, of a potential mate. So your behavioral response to that guy in the bar may be based not only on your own hormones, but his, too.
I am grateful to Chris Goode, Ellen Cho, Henry Lange, Ben Solomon, and Greg Ball for their contributions to this work, which is supported by NSF IBN-0346984.
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About the Author
Donna L. Maney earned her PhD in Neurobiology and Behavior from the University of Washington in 1997 and did her post-doctoral work in the Department of Psychological and Brain Sciences at Johns Hopkins University. She is currently an Assistant Professor of Psychology and a member of the Graduate Program in Neuroscience at Emory University in Atlanta, GA. Her research focuses on the sensory physiology and neuroendocrinology of auditory communication, using songbirds as model systems. Other research interests include the genetic bases of social behavior, particularly the interactions between genes, neuropeptides, steroid hormones and the environment as they relate to behavior. She is a recipient of the Presidential Early Career Award for Scientists and Engineers (2004) and her research is funded by a CAREER award from the National Science Foundation.