The ability of steroid hormones to rapidly influence cell physiology through nongenomic mechanisms raises the possibility that these molecules may play a role in the dynamic regulation of social behavior, particularly in species in which social stimuli can rapidly influence circulating steroid levels. We therefore tested if testosterone (T), which increases in male goldfish in response to sexual stimuli, can rapidly influence approach responses towards females. Injections of T stimulated approach responses towards the visual cues of females 30–45 min after the injection but did not stimulate approach responses towards stimulus males or affect general activity, indicating that the effect is stimulus-specific and not a secondary consequence of increased arousal. Estradiol produced the same effect 30–45 min and even 10–25 min after administration, and treatment with the aromatase inhibitor fadrozole blocked exogenous T's behavioral effect, indicating that T's rapid stimulation of visual approach responses depends on aromatization. We suggest that T surges induced by sexual stimuli, including preovulatory pheromones, rapidly prime males to mate by increasing sensitivity within visual pathways that guide approach responses towards females and/or by increasing the motivation to approach potential mates through actions within traditional limbic circuits.
Social stimuli, particularly aggressive and sexual stimuli, often stimulate rapid increases in sex hormones in vertebrate animals. Such acute changes in sex steroid levels can influence subsequent social encounters, likely through genomic mechanisms that involve changes in gene transcription associated with intracellular steroid receptors (Trainor et al., 2004). Additionally, such steroid elevations may modulate the immediate expression of ongoing behavior through more rapid mechanisms mediated by membrane receptors (reviewed in Balthazart and Ball, 2006 and Bass and Remage-Healey, 2008). Thus, in addition to slowly sculpting neural pathways associated with behavioral control, sex steroids are also capable of acting as dynamic regulators of those pathways through rapid, nongenomic mechanisms.
However, with the exception of work in toadfish and plainfin midshipmen showing that sex steroids can rapidly influence hindbrain pattern generators involved in the production of motor output related to social communication (Remage-Healey and Bass, 2006 and Remage-Healey and Bass, 2007), very little is known about where and how within the brain sex steroids act to rapidly influence social behavior. One interesting possibility is that sex steroids may rapidly modulate sensory mechanisms that facilitate the processing of social stimuli. It has been demonstrated that chronic steroid treatments can influence how animals perceive sensory information related to social communication by acting on early stages of sensory detection and processing. For example, chronic androgen treatment alters the tuning of primary electroreceptive sensory afferents in weakly electric fish (Keller et al., 1986) and stingrays (Sisneros and Tricas, 2000) and selectively increases the magnitude and sensitivity of the electro-olfactogram response to a putative sex pheromone in a Southeast Asian cyprinid, the tinfoil barb (Cardwell et al., 1995). However, it is not known whether sex steroids can rapidly modulate sensory processes and thus influence social perception in ways that have immediate behavioral consequences.
The importance of olfactory signals for social communication has been well described in many vertebrate species, including goldfish. However, visual cues are also important for social communication in this species, particularly in sexual contexts. Male goldfish follow ovulating females more than nonovulating females, even after ablation of the olfactory tract (Partridge et al., 1976), and males preferentially approach female over male visual stimuli in choice tests during the breeding season (Thompson et al., 2004). That visual processes related to reproduction may be influenced by sex steroids is suggested by the presence of high levels of aromatase, as well as androgen and estrogen receptors, in regions of the brain involved in the detection of (retina) and orientation towards (optic tectum) visual stimuli (Gelinas and Callard, 1993 and Gelinas and Callard, 1997). In fact, androgen treatments that masculinize reproductive behavior in female goldfish also induce selective approach responses towards female visual stimuli (Thompson et al., 2004). Interestingly, exposure to preovulatory females causes a T surge in males (Kobayashi et al., 1986) that could rapidly influence those visual responses. We therefore tested if T can rapidly influence male approach responses towards females in an experimental paradigm in which only visual cues were present. To determine the biochemical pathway associated with any such influences, we also tested whether T produces rapid behavioral effects through its conversion by aromatase to estradiol (E2).
