Abstract
Catecholaminergic (CA) neurons innervate sensory areas and affect the processing of sensory signals. For example, in birds, CA fibers innervate the auditory pathway at each level, including the midbrain, thalamus, and forebrain. We have shown previously that in female European starlings, CA activity in the auditory forebrain can be enhanced by exposure to attractive male song for one week. It is not known, however, whether hearing song can initiate that activity more rapidly. Here, we exposed estrogen-primed, female white-throated sparrows to conspecific male song and looked for evidence of rapid synthesis of catecholamines in auditory areas. In one hemisphere of the brain, we used immunohistochemistry to detect the phosphorylation of tyrosine hydroxylase (TH), a rate-limiting enzyme in the CA synthetic pathway. We found that immunoreactivity for TH phosphorylated at serine 40 increased dramatically in the auditory forebrain, but not the auditory thalamus and midbrain, after 15 min of song exposure. In the other hemisphere, we used high pressure liquid chromatography to measure catecholamines and their metabolites. We found that two dopamine metabolites, dihydroxyphenylacetic acid and homovanillic acid, increased in the auditory forebrain but not the auditory midbrain after 30 min of exposure to conspecific song. Our results are consistent with the hypothesis that exposure to a behaviorally relevant auditory stimulus rapidly induces CA activity, which may play a role in auditory responses.
Highlights
The processes of attending to a stimulus and assigning value to it both depend on catecholamine neuromodulators such as dopamine (DA) and norepinephrine (NE)
We looked for evidence of rapid increases in catecholamine synthesis in auditory areas of sexually receptive females listening to conspecific male song
Fifteen min of song exposure caused an increase in phosphorylated TH (pTH) immunoreactivity in the auditory forebrain, indicating the rapid engagement of catecholaminergic synthetic machinery (Fig. 3). pTH immunoreactivity increased in both NCM and caudomedial mesopallium (CMM) after 15 min of song exposure (NCM: z = 5.20, P,0.001; CMM: z = 5.35, P,0.001) and after 30 min of song exposure was still elevated above baseline in NCM (z = 2.16, P = 0.031)
Summary
The processes of attending to a stimulus and assigning value to it both depend on catecholamine neuromodulators such as dopamine (DA) and norepinephrine (NE). Catecholaminergic (CA) systems can alter sensory gating and receptive fields to maximize the salience of behaviorally relevant signals. In so doing, they serve as dynamic filters that integrate prior experience, environmental context, and internal state [1,2]. In female white-throated sparrows (Zonotrichia albicollis), sexual receptivity is associated with an increase in the number of CA neurons in brainstem cell groups likely to project to auditory areas [10], as well as denser CA innervation of the auditory forebrain and midbrain [10,19]. There is evidence that catecholaminergic projections to auditory areas may carry information on internal state and social context, that these projections regulate behavioral and neural responses to song, and that hearing song may itself alter catecholamine levels in the auditory system
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