During acoustic communication, animals must attend to sounds from a particular source while simultaneously rejecting intrusion from other sources. One possible candidate mechanism for this process is the noradrenergic system. Noradrenaline is a neuromodulator that tunes sensory processing systems and regulates attention. We examined whether pharmacological degradation of the noradrenergic system using N-(2-chloroethyl)-N-2-bromobenzyl-amine hydrochloride (DSP-4) modifies processing of species-typical auditory signals in female canaries (Serinus canaria). We measured auditory responses to conspecific and heterospecific songs using ZENK protein expression within the caudomedial nidopallium (NCM) and the mesopallium caudomedial (CMM). Song-induced ZENK expression in these auditory forebrain areas is typically higher in birds exposed to conspecific songs as opposed to heterospecific songs. Our results reveal that this differential ZENK induction is abolished specifically within dNCM and CMM in female canaries treated with DSP-4. Furthermore, in DSP-4-treated birds, conspecific song-induced ZENK expression is significantly reduced when compared to saline-treated birds. This suggests that the noradrenergic system modifies auditory processing by enhancing neuronal responses to signals relevant to survival and reproduction rather than inhibiting neuronal responses to signals that are less relevant. Overall, our results reveal that noradrenaline plays a significant neuromodulatory role during the reception of species-typical communication signals.

1.
Appeltants D, Del Negro C, Balthazart J (2002) Noradrenergic control of auditory information processing in female canaries. Behav Brain Res 133:221–235.
2.
Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403–450.
3.
Aston-Jones G, Rajkowski J, Cohen J (2000) Locus coeruleus and regulation of behavioral flexibility and attention. Prog Brain Res 126:165–182.
4.
Bailey DJ, Rosebush JC, Wade J (2002) The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J Neurobiol 52:43 – 51.
5.
Bailey WJ, Morris GK (1986) Confusion of phonotaxis by masking sounds in the bushcricket Conocephalus brevipennis (Tettigoniidae:Conocephalinae). Ethology 73:19–28.
6.
Balthazart J, Libioulle JM, Sante P (1988) Stimulatory effects of the noradrenergic neurotoxin DSP-4 on sexual behavior in male quail. Behav Proc 17:27–44.
7.
Barclay SR, Harding CF, Waterman SA (1992) Correlations between catecholamine levels and sexual behavior in male zebra finches. Pharmacol Biochem Behav 41:195–201.
8.
Barclay SR, Harding CF, Waterman SA (1996) Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol Biochem Behav 53:213–220.
9.
Berridge CW, Waterhouse BD (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42:33–84.
10.
Cardin J, Schmidt M (2004a) Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 24:7745–7753.
11.
Cardin J, Schmidt M (2004b) Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J Neurophysiol 91:2148–63.
12.
Castelino CB, Ball GF (2005) The role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur J Neurosci 21:1962–1972.
13.
Charlier TD, Ball GF, Balthazart J (2005) Sexual behavior activates the expression of the immediate early genes c-fos and Zenk (egr-1) in catecholaminergic neurons of male Japanese quail. Neuroscience 131:13–30.
14.
Cherry EC (1953) Some experiments on recognition of speech, with one and two ears. J Acoust Soc Am 25:975–979.
15.
Duffy DL, Bentley GE, Ball GF (1999) Does sex or photoperiodic condition influence ZENK induction in response to song in European starlings? Brain Res 844:78–82.
16.
Ehret G, Gerhardt HC (1980) Auditory masking and effects of noise on responses of the green treefrog (Hyla cinerea) to synthetic mating calls. J Comp Physiol 141:13–18.
17.
Gentner TQ, Hulse SH (2000) Female European Starlings preference and choice for variation in conspecific male song. Anim Behav 59:443–458.
18.
Gentner TQ, Hulse SH, Duffy D, Ball GF (2001) Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46:48–58.
19.
Hoke KL, Ryan MJ, Wilczynski W (2006) Social cues shift functional connectivity in the hypothalamus. Proc Natl Acad Sci USA 102:10712–10717.
20.
Jarvis ED, Nottebohm F (1997) Motor-driven gene expression. Proc Natl Acad Sci USA 94:4097–4102.
21.
Leitner S, Voigt C, Metzdorf R, Catchpole CK (2005) Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J Neurobiol 64:275–284.
22.
Lynch KS, Wilczynski W (2008) Reproductive hormones modify reception of species-typical communication signals in a female Anuran. Brain Behav Evol 71:143–150.
23.
Maney DL, Ball GF (2003) Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J Neurobiol 56:163–170.
24.
Maney DL, MacDougall-Shackleton EA, MacDougall-Shackleton SA, Ball GF, Hahn TP (2003) Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 9:667–674.
25.
Mello CV, Vicario DS, Clayton DF (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci USA 89:6818–6822.
26.
Mello CV, Clayton DF (1994) Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14:6652–6666.
27.
Mello CV, Pinaud R, Ribeiro S (1998) Noradrenergic system of the zebra finch brain: immunocytochemical study of dopamine-beta-hydroxylase. J Comp Neurol 400:207–228.
28.
Mello CV, Ribeiro S (1998) ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393:426–438.
29.
Mello CV (2002) Mapping vocal communication pathways in birds with inducible gene expression. J Comp Physiol A 188:943–959.
30.
Riters LV, Algers SJ (2004) Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song. Cell Tissue Res 316:35–44.
31.
Riters LV, Pawlisch BA (2007) Evidence that norepinephrine influences responses to male courtship song and activity within song control regions and the ventromedial nucleus of the hypothalamus in female European starlings. Brain Res 1149:127–140.
32.
Sockman KW, Gentner TQ, Ball GF (2002) Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc R Soc Lond B 269:2479–2485.
33.
Stripling R, Kruse AA, Clayton DF (2001) Development of song responses in the zebra finch caudomedial neostriatum: role of genomic and electrophysiological activities. J Neurobiol 48:163–180.
34.
Taziaux M, Lopez J, Cornil CA, Balthazart J, Holloway KS (2007) Differential c-fos expression in the brain of male Japanese quail following exposure to stimuli that predict or do not predict the arrival of a female. Eur J Neurosci 25:2835–2846.
35.
Terleph TA, Mello CV, Vicario DS (2006) Auditory topography and temporal response dynamics of canary caudal telencephalon. J Neurobiol 66:281–292.
36.
Terpstra NJ, Bolhuis JJ, Riebel K, Van der Berg JM, Boer-Visser A (2006) Localized brain activation specific to auditory memory in a female songbird. J Comp Neurol 494:784–791.
37.
Velho TAF, Ribeiro S, Pinaud R, Mello CV (2006) Noradrenergic modulation of song-induced gene expression in the caudomedial nidopallium (NCM) of zebra finches Soc Neurosci Abst 374.12
38.
Wiley RH (1994) Errors, exaggeration and deception in animal communication. In: Behavioral Mechanisms in Evolutionary Ecology (Real L, ed), pp 157–189. Chicago, IL: University of Chicago Press.
39.
Wiley RH (2006) Signal detection and animal communication. In: Advances in the Study of Behavior (Brockman HJ, Slater P, Snowdon C, Roper T, Naguib M, Wynne-Edward K, eds.), vol. 36, pp 217–247. Amsterdam:Elsevier Academic Press.
40.
Wollerman L, Wiley RH (2001) Background noise from a natural chorus alters female discrimination of male calls in a Neotropical frog. Anim Behav 62:1–8.
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