Socially induced serotonergic fluctuations in the male auditory midbrain correlate with female behavior during courtship

Abstract

Keesom SM, Hurley LM. Socially induced serotonergic fluctuations in the male auditory midbrain correlate with female behavior during courtship. J Neurophysiol 115: 1786 -1796, 2016. First published January 20, 2016 doi:10.1152/jn.00742.2015.-Cues from social partners trigger the activation of socially responsive neuromodulatory systems, priming brain regions including sensory systems to process these cues appropriately. The fidelity with which neuromodulators reflect the qualities of ongoing social interactions in sensory regions is unclear. We addressed this issue by using voltammetry to monitor serotonergic fluctuations in an auditory midbrain nucleus, the inferior colliculus (IC), of male mice (Mus musculus) paired with females, and by concurrently measuring behaviors of both social partners. Serotonergic activity strongly increased in male mice as they courted females, relative to serotonergic activity in the same males during trials with no social partners. Across individual males, average changes in serotonergic activity were negatively correlated with behaviors exhibited by female partners, including broadband squeaks, which relate to rejection of males. In contrast, serotonergic activity did not correlate with male behaviors, including ultrasonic vocalizations. These findings suggest that during courtship, the level of serotonergic activity in the IC of males reflects the valence of the social interaction from the perspective of the male (i.e., whether the female rejects the male or not). As a result, our findings are consistent with the hypothesis that neuromodulatory effects on neural responses in the IC may reflect the reception, rather than the production, of vocal signals.

Sound‐induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally‐breeding songbird

“…First, we measured monoamine turnover in dissected tissue, which does not afford the best time resolution. Methods of measuring release in real time, such as voltammetry, should be employed to better detect event‐related release. Second, our definition of monoamine turnover is based on the assumption that an increase in metabolites, relative to the concentration of the monoamines themselves, indicates release.…”

Serotonin modulates response properties of neurons in the dorsal cochlear nucleus of the mouse

“…This notion is supported by the fact that fusiform cells respond selectively to some conspecific vocalizations over others and are in a position to transmit this information directly to the IC (Roberts and Portfors, 2015), where further processing occurs (Klug et al, 2002; Hurley and Pollak, 2005a; Portfors et al, 2009; Holmstrom et al, 2010). Behaviorally important interactions, such as courtship or stress caused by the presence of an intruder, lead to changes in 5-HT levels in the IC and this is thought to affect the reception of vocalizations (Hall et al, 2011; Keesom and Hurley, 2016). Based on the current findings in the DCN, the serotonergic system is capable of modulating the excitability of neurons at low levels of the ascending auditory pathway, potentially affecting the salience of vocalizations depending on arousal state, attention, and behavioral context.…”

Social experience alters socially induced serotonergic fluctuations in the inferior colliculus

“…All CFEs were electrically and chemically pretreated to increase sensitivity to and selectivity for serotonin, as described previously (Hall et al 2010;Keesom and Hurley 2016). CFEs were electrically pretreated by suspension in phosphate-citrate buffer and application of the following protocol (vs. a Ag-AgCl reference electrode and a calomel auxiliary electrode), using an eCorder controlled by Chart software (eDAQ, Denistone East, NSW, Australia): 70 Hz, 0.3 V triangle waveform for 30 s, 1.5 V for 10 s, Ϫ0.5 V for 5 s, and 1.5 V for 8 s. This pretreatment separated the oxidation potentials of ascorbic acid, catecholamines, and serotonin into three discernible peaks on a plot of applied voltage vs. the first derivative of the current.…”

“…Serotonergic fibers innervate the majority of brain regions, including primary sensory regions, and serotonin that is endogenously released or exogenously applied to sensory regions modulates sensory responses, including olfactory (Lottem et al 2016), electrosensory (Deemyad et al 2013), and auditory processing (Hurley and Sullivan 2012). Finally, serotonergic activity within sensory regions such as the auditory midbrain is graded with the intensity of behavioral interaction in subject males interacting with either males or females (Hall et al 2011;Keesom and Hurley 2016).…”

“…Furthermore, the use of these signals is altered by social experience (Chabout et al 2012;Keesom et al 2017). In the inferior colliculus (IC), a mammalian auditory midbrain nucleus, endogenous fluctuations in serotonergic activity during social encounters between mice correlate with behavior (Hall et al 2011;Hanson and Hurley 2014;Keesom and Hurley 2016). This suggests that auditory neuromodulation by serotonin could depend on features of context, because serotonin regulates how IC neurons respond to vocalizations (Hurley and Pollak 2005).…”