Song Competition Affects Monoamine Levels in Sensory and Motor Forebrain Regions of Male Lincoln's Sparrows (Melospiza lincolnii)

Abstract

Male animals often change their behavior in response to the level of competition for mates. Male Lincoln's sparrows (Melospiza lincolnii) modulate their competitive singing over the period of a week as a function of the level of challenge associated with competitors' songs. Differences in song challenge and associated shifts in competitive state should be accompanied by neural changes, potentially in regions that regulate perception and song production. The monoamines mediate neural plasticity in response to environmental cues to achieve shifts in behavioral state. Therefore, using high pressure liquid chromatography with electrochemical detection, we compared levels of monoamines and their metabolites from male Lincoln's sparrows exposed to songs categorized as more or less challenging. We compared levels of norepinephrine and its principal metabolite in two perceptual regions of the auditory telencephalon, the caudomedial nidopallium and the caudomedial mesopallium (CMM), because this chemical is implicated in modulating auditory sensitivity to song. We also measured the levels of dopamine and its principal metabolite in two song control nuclei, area X and the robust nucleus of the arcopallium (RA), because dopamine is implicated in regulating song output. We measured the levels of serotonin and its principal metabolite in all four brain regions because this monoamine is implicated in perception and behavioral output and is found throughout the avian forebrain. After controlling for recent singing, we found that males exposed to more challenging song had higher levels of norepinephrine metabolite in the CMM and lower levels of serotonin in the RA. Collectively, these findings are consistent with norepinephrine in perceptual brain regions and serotonin in song control regions contributing to neuroplasticity that underlies socially-induced changes in behavioral state.

Sex Differences in Forebrain Monoaminergic Response to Song Performance

“…Approximately 85 songs played per 20-min interval, and approximately 890 songs played over the entire 5.25 h of song exposure. Songs played at a peak amplitude of 70 dB 5 cm from the speaker [Sewall et al, 2013;Lyons et al, 2014].…”

“…From the 300-μm sections, we used micropunches to collect tissue in CMM and NCM, using Field L as a guide as described previously [Sewall et al, 2013]. We collected a 0.5-mm diameter section from CMM and a 1-mm diameter section from NCM.…”

“…We used methodology described previously [Sewall et al, 2013] to quantify monoamines and their metabolites by HPLC-ECD. We added 100 μL of mobile phase to each tissue sample tube.…”

“…We used bovine serum albumin as a standard and performed all analyses on an UQuant microplate spectrophotometer (BioTek, Winooski, VT, USA). In situations in which the protein assay was unreliable and we were not able to repeat it due to low sample volume, we followed the protocol established previously [Sewall et al, 2013], and estimated the amount of protein as the average of the amount in the other tissue samples from the same brain region (CMM = 1 male, NCM = 3 females).…”

“…Norepinephrine regulates attention and memory formation throughout sensory systems by increasing the signal-to-noise ratio of neuronal responses to sensory stimuli [Oades, 1985;Aston-Jones and Cohen, 2005;Sara, 2009;Castelino and Schmidt, 2010]. One or all of these monoamines may be involved in modulating sensory perception in response to experience with the value of a sexual signal [Sockman, 2007;Salvante et al, 2009;Sewall et al, 2013]. However, because the valence of sexual signals differs between the sexes, we predicted that the monoaminergic responses to sexual signals would also differ.…”