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Neuroanatomical Evidence for Catecholamines as Modulators of Audition and Acoustic Behavior in a Vocal Teleost

  • Chapter
Fish Hearing and Bioacoustics

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 877))

Abstract

The plainfin midshipman fish (Porichthys notatus) is a well-studied model to understand the neural and endocrine mechanisms underlying vocal-acoustic communication across vertebrates. It is well established that steroid hormones such as estrogen drive seasonal peripheral auditory plasticity in female Porichthys in order to better encode the male’s advertisement call. However, little is known of the neural substrates that underlie the motivation and coordinated behavioral response to auditory social signals. Catecholamines, which include dopamine and noradrenaline, are good candidates for this function, as they are thought to modulate the salience of and reinforce appropriate behavior to socially relevant stimuli. This chapter summarizes our recent studies which aimed to characterize catecholamine innervation in the central and peripheral auditory system of Porichthys as well as test the hypotheses that innervation of the auditory system is seasonally plastic and catecholaminergic neurons are activated in response to conspecific vocalizations. Of particular significance is the discovery of direct dopaminergic innervation of the saccule, the main hearing end organ, by neurons in the diencephalon, which also robustly innervate the cholinergic auditory efferent nucleus in the hindbrain. Seasonal changes in dopamine innervation in both these areas appear dependent on reproductive state in females and may ultimately function to modulate the sensitivity of the peripheral auditory system as an adaptation to the seasonally changing soundscape. Diencephalic dopaminergic neurons are indeed active in response to exposure to midshipman vocalizations and are in a perfect position to integrate the detection and appropriate motor response to conspecific acoustic signals for successful reproduction.

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References

  • Adrio F, Anadon R, Rodriguez-Moldes I (2002) Distribution of tyrosine hydroxylase (TH) and dopamine beta-hydroxylase (DBH) immunoreactivity in the central nervous system of two chondrostean fishes (Acipenser baeri and Huso huso). J Comp Neurol 448(3):280–297. doi:10.1002/cne.10256

    Article  CAS  PubMed  Google Scholar 

  • Alderks PW, Sisneros JA (2013) Development of the acoustically evoked behavioral response in larval plainfin midshipman fish, Porichthys notatus. PLoS One 8(12), e82182. doi:10.1371/journal.pone.0082182

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ampatzis K, Dermon CR (2010) Regional distribution and cellular localization of beta2-adrenoceptors in the adult zebrafish brain (Danio rerio). J Comp Neurol 518(9):1418–1441. doi:10.1002/cne.22278

    Article  CAS  PubMed  Google Scholar 

  • Ampatzis K, Kentouri M, Dermon CR (2008) Neuronal and glial localization of alpha(2A)-adrenoceptors in the adult zebrafish (Danio rerio) brain. J Comp Neurol 508(1):72–93. doi:10.1002/cne.21663

    Article  CAS  PubMed  Google Scholar 

  • Appeltants D, Ball GF, Balthazart J (2001) The distribution of tyrosine hydroxylase in the canary brain: demonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nulcei. Cell Tissue Res 304(2):237–259

    Article  CAS  PubMed  Google Scholar 

  • Appeltants D, Del Negro C, Balthazart J (2002) Noradrenergic control of auditory information processing in female canaries. Behav Brain Res 133(2):221–235. pii: S0166432802000050

    Google Scholar 

  • Bass AH (1996) Shaping brain sexuality. Am Sci 84(4):352–363

    Google Scholar 

  • Bass AH, Baker R (1990) Sexual dimorphisms in the vocal control system of a teleost fish: morphology of physiologically identified neurons. J Neurobiol 21(8):1155–1168

    Article  CAS  PubMed  Google Scholar 

  • Bass AH, Clark C (2003) The physical acoustics of underwater sound communication. In: Simmons AM, Popper AN, Fay RR (eds) Handbook of auditory research, vol 16. Springer, New York, pp 15–64

    Google Scholar 

  • Bass AH, McKibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Prog Neurobiol 69(1):1–26

    Article  PubMed  Google Scholar 

  • Bass AH, Marchaterre MA, Baker R (1994) Vocal-acoustic pathways in a teleost fish. J Neurosci 14(7):4025–4039

    CAS  PubMed  Google Scholar 

  • Bass AH, Bodnar DA, Marchaterre MA (1999) Complementary explanations for existing phenotypes in an acoustic communication system. In: Hauser M, Konishi M (eds) Neural mechanisms of communication. MIT Press, Cambridge, pp 493–514

    Google Scholar 

  • Bass AH, Bodnar DA, Marchaterre MA (2000) Midbrain acoustic circuitry in a vocalizing fish. J Comp Neurol 419(4):505–531

    Article  CAS  PubMed  Google Scholar 

  • Bass AH, Bodnar DA, Marchaterre MA (2001) Acoustic nuclei in the medulla and midbrain of the vocalizing gulf toadfish (Opsanus beta). Brain Behav Evol 57(2):63–79

    Article  CAS  PubMed  Google Scholar 

  • Bass AH, Rose GJ, Pritz MB (2005) Auditory midbrain of fish, amphibians and reptiles: models systems for understanding auditory function. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 459–492

    Chapter  Google Scholar 

  • Batten TF, Berry PA, Maqbool A, Moons L, Vandesande F (1993) Immunolocalization of catecholamine enzymes, serotonin, dopamine and L-dopa in the brain of Dicentrarchus labrax (Teleostei). Brain Res Bull 31(3–4):233–252. pii: 0361-9230(93)90214-V

    Google Scholar 

  • Berridge CW (2008) Noradrenergic modulation of arousal. Brain Res Rev 58(1):1–17. doi:10.1016/j.brainresrev.2007.10.013

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berridge CW, Waterhouse BD (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42(1):33–84. pii: S0165017303001437

    Google Scholar 

  • Bodnar DA, Bass AH (1997) Temporal coding of concurrent acoustic signals in auditory midbrain. J Neurosci 17(19):7553–7564

    CAS  PubMed  Google Scholar 

  • Bodnar DA, Bass AH (1999) Midbrain combinatorial code for temporal and spectral information in concurrent acoustic signals. J Neurophysiol 81(2):552–563

    CAS  PubMed  Google Scholar 

  • Braford MR Jr, Northcutt RG (1983) Organization of the diencephalon and pretectum of the ray-finned fishes. In: Davis RE, Northcutt RG (eds) Fish neurobiology. University of Michigan Press, Ann Arbor, pp 117–164

    Google Scholar 

  • Brantley RK, Bass AH (1988) Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase. J Comp Neurol 275(1):87–105

    Article  CAS  PubMed  Google Scholar 

  • Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic-signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96(3):213–232

    Article  Google Scholar 

  • Brantley RK, Wingfield JC, Bass AH (1993) Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism among teleost fishes. Horm Behav 27(3):332–347

    Article  CAS  PubMed  Google Scholar 

  • Bricaud O, Chaar V, Dambly-Chaudiere C, Ghysen A (2001) Early efferent innervation of the zebrafish lateral line. J Comp Neurol 434(3):253–261

    Article  CAS  PubMed  Google Scholar 

  • Caras ML (2013) Estrogenic modulation of auditory processing: a vertebrate comparison. Front Neuroendocrinol 34(4):285–299. doi:10.1016/j.yfrne.2013.07.006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chagnaud BP, Bass AH (2013) Vocal corollary discharge communicates call duration to vertebrate auditory system. J Neurosci 33(48):18775–18780. doi:10.1523/JNEUROSCI.3140-13.2013

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chagnaud BP, Baker R, Bass AH (2011) Vocalization frequency and duration are coded in separate hindbrain nuclei. Nat Commun 2:346. doi:10.1038/ncomms1349

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Coffin AB, Mohr RA, Sisneros JA (2012) Saccular-specific hair cell addition correlates with reproductive state-dependent changes in the auditory saccular sensitivity of a vocal fish. J Neurosci 32(4):1366–1376. doi:10.1523/JNEUROSCI.4928-11.2012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen MJ, Winn HE (1967) Electrophysiological observations on hearing and sound production in the fish, Porichthys notatus. J Exp Zool 165:355–370

    Article  CAS  PubMed  Google Scholar 

  • Corio M, Peute J, Steinbusch HW (1991) Distribution of serotonin- and dopamine-immunoreactivity in the brain of the teleost Clarias gariepinus. J Chem Neuroanat 4(2):79–95. pii: 0891-0618(91)90033-9

    Google Scholar 

  • Edeline JM, Manunta Y, Hennevin E (2011) Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation. Hear Res 274(1-2):75–84. doi:10.1016/j.heares.2010.08.005

    Article  PubMed  Google Scholar 

  • Ekstrom P, Reschke M, Steinbusch H, van Veen T (1986) Distribution of noradrenaline in the brain of the teleost Gasterosteus aculeatus L.: an immunohistochemical analysis. J Comp Neurol 254(3):297–313. doi:10.1002/cne.902540304

    Article  CAS  PubMed  Google Scholar 

  • Ekstrom P, Honkanen T, Steinbusch HW (1990) Distribution of dopamine-immunoreactive neuronal perikarya and fibres in the brain of a teleost, Gasterosteus aculeatus L. comparison with tyrosine hydroxylase- and dopamine-beta-hydroxylase-immunoreactive neurons. J Chem Neuroanat 3(4):233–260

    CAS  PubMed  Google Scholar 

  • Endepols H, Walkowiak W, Luksch H (2000) Chemoarchitecture of the anuran auditory midbrain. Brain Res Brain Res Rev 33(2–3):179–198. pii: S0165017300000291

    Google Scholar 

  • Fay RR, Edds-Walton PL (2008) Structures and functions of the auditory nervous system of fishes. In: Webb JF, Fay RR, Popper AN (eds) Fish bioacoustics, vol 32, Springer handbook of auditory research. Springer, New York, pp 49–97

    Chapter  Google Scholar 

  • Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809–834

    Article  CAS  PubMed  Google Scholar 

  • Filippi A, Mahler J, Schweitzer J, Driever W (2010) Expression of the paralogous tyrosine hydroxylase encoding genes Th1 and Th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. J Comp Neurol 518(4):423–438. doi:10.1002/cne.22213

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fine ML, Lenhardt ML (1983) Shallow-water propagation of the toadfish mating call. Comp Biochem Physiol A Comp Physiol 76(2):225–231

    Article  CAS  PubMed  Google Scholar 

  • Fine ML, Perini MA (1994) Sound production evoked by electrical stimulation of the forebrain in the oyster toadfish. J Comp Physiol A 174(2):173–185

    Article  CAS  PubMed  Google Scholar 

  • Forlano PM, Bass AH (2011) Neural and hormonal mechanisms of reproductive-related arousal in fishes. Horm Behav 59(5):616–629. doi:10.1016/j.yhbeh.2010.10.006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Forlano PM, Kim SD, Krzyminska ZM, Sisneros JA (2014) Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish Porichthys notatus. J Comp Neurol 522(13):2887–2927. doi:10.1002/cne.23596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Forlano PM, Ghahramani ZN, Monestime CM, Kurochkin P, Chernenko A, Milkis D (2015a) Catecholaminergic innervation of central and peripheral auditory circuitry varies with reproductive state in female midshipman fish, Porichthys notatus. PLoS One 10(4), e0121914. doi: 10.1371/journal.pone.0121914

    Google Scholar 

  • Forlano PM, Sisneros JA, Rohmann KN, Bass AH (2015b) Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish. Front Neuroendocrinol 37:129–145. doi:10.1016/j.yfrne.2014.08.002

    Article  CAS  PubMed  Google Scholar 

  • Furukawa T (1981) Effects of efferent stimulation on the saccule of goldfish. J Physiol 315:203–215

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garrett AR, Robertson D, Sellick PM, Mulders WH (2011) The actions of dopamine receptors in the guinea pig cochlea. Audiol Neurootol 16(3):145–157. doi:10.1159/000316674

    Article  CAS  PubMed  Google Scholar 

  • Genova RM, Marchaterre MA, Knapp R, Fergus D, Bass AH (2013) Glucocorticoid and androgen signaling pathways diverge between advertisement calling and non-calling fish. Horm Behav 62(4):426–432. doi:10.1016/j.yhbeh.2012.07.010

    Article  CAS  Google Scholar 

  • Gittelman JX, Perkel DJ, Portfors CV (2013) Dopamine modulates auditory responses in the inferior colliculus in a heterogeneous manner. J Assoc Res Otolaryngol 14(5):719–729. doi:10.1007/s10162-013-0405-0

    Article  PubMed Central  PubMed  Google Scholar 

  • Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48(1):11–22

    Article  PubMed Central  PubMed  Google Scholar 

  • Goodson JL, Bass AH (2002) Vocal-acoustic circuitry and descending vocal pathways in teleost fish: convergence with terrestrial vertebrates reveals conserved traits. J Comp Neurol 448(3):298–322

    Article  PubMed  Google Scholar 

  • Goodson JL, Kabelik D (2009) Dynamic limbic networks and social diversity in vertebrates: from neural context to neuromodulatory patterning. Front Neuroendocrinol 30(4):429–441. doi:10.1016/j.yfrne.2009.05.007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goodson JL, Kingsbury MA (2013) What’s in a name? Considerations of homologies and nomenclature for vertebrate social behavior networks. Horm Behav 64(1):103–112. doi:10.1016/j.yhbeh.2013.05.006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hornby PJ, Piekut DT (1990) Distribution of catecholamine-synthesizing enzymes in goldfish brains: presumptive dopamine and norepinephrine neuronal organization. Brain Behav Evol 35(1):49–64

    Article  CAS  PubMed  Google Scholar 

  • Hurley LM, Devilbiss DM, Waterhouse BD (2004) A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr Opin Neurobiol 14(4):488–495. pii: S0959-4388(04)00096-0

    Google Scholar 

  • Ibara RM, Penny LT, Ebeling AW, van Dykhuizen D, Cailliet G (1983) The mating call of the plainfin midshipman fish, Porichthys notatus. In: Noakes DLG, Lundquist DG, Helfman GS, Ward JA (eds) Predators and prey in fishes. Dr. W. Junk Publishers, The Hague, pp 205–212

    Chapter  Google Scholar 

  • Joshua M, Adler A, Bergman H (2009) The dynamics of dopamine in control of motor behavior. Curr Opin Neurobiol 19(6):615–620. doi:10.1016/j.conb.2009.10.001

    Article  CAS  PubMed  Google Scholar 

  • Kapsimali M, Vidal B, Gonzalez A, Dufour S, Vernier P (2000) Distribution of the mRNA encoding the four dopamine D(1) receptor subtypes in the brain of the european eel (Anguilla anguilla): comparative approach to the function of D(1) receptors in vertebrates. J Comp Neurol 419(3):320–343. doi:10.1002/(SICI)1096-9861(20000410)419:3<320::AID-CNE5>3.0.CO;2-F

    Google Scholar 

  • Kaslin J, Panula P (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J Comp Neurol 440(4):342–377. doi:10.1002/cne.1390

    Google Scholar 

  • Kastenhuber E, Kratochwil CF, Ryu S, Schweitzer J, Driever W (2010) Genetic dissection of dopaminergic and noradrenergic contributions to catecholaminergic tracts in early larval zebrafish. J Comp Neurol 518(4):439–458. doi:10.1002/cne.22214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kelly AM, Goodson JL (2015) Functional interactions of dopamine cell groups reflect personality, sex, and social context in highly social finches. Behav Brain Res 280:101–112. doi:10.1016/j.bbr.2014.12.004

    Article  CAS  PubMed  Google Scholar 

  • Kirk EC, Smith DW (2003) Protection from acoustic trauma is not a primary function of the medial olivocochlear efferent system. J Assoc Res Otolaryngol 4(4):445–465. doi:10.1007/s10162-002-3013-y

    Article  Google Scholar 

  • Kittelberger JM, Bass AH (2013) Vocal-motor and auditory connectivity of the midbrain periaqueductal gray in a teleost fish. J Comp Neurol 521(4):791–812. doi:10.1002/cne.23202

    Article  PubMed Central  PubMed  Google Scholar 

  • Kittelberger M, Land BR, Bass AH (2006) Midbrain periaqueductal gray and vocal pattering in a teleost fish. J Neurophysiol 96:71–85

    Article  PubMed  Google Scholar 

  • Klepper A, Herbert H (1991) Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Res 557(1–2):190–201. pii: 0006-8993(91)90134-H

    Google Scholar 

  • Knapp R, Wingfield JC, Bass AH (1999) Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus). Horm Behav 35(1):81–89

    Article  CAS  PubMed  Google Scholar 

  • Koppl C (2011) Evolution of the octavolateralis efferent system. In: Ryugo DK, Fay RR, Popper AN (eds) Auditory and vestibular efferents. Springer, New York, pp 217–259

    Chapter  Google Scholar 

  • Kossl M, Vater M (1989) Noradrenaline enhances temporal auditory contrast and neuronal timing precision in the cochlear nucleus of the mustached bat. J Neurosci 9(12):4169–4178

    CAS  PubMed  Google Scholar 

  • Lagardere JP, Ernande B (2004) Sounds recorded in salt marshes and attributed to the European eel. C R Biol 327(4):353–359

    Article  PubMed  Google Scholar 

  • Lendvai B, Halmos GB, Polony G, Kapocsi J, Horvath T, Aller M, Sylvester Vizi E, Zelles T (2011) Chemical neuroprotection in the cochlea: the modulation of dopamine release from lateral olivocochlear efferents. Neurochem Int 59(2):150–158. doi:10.1016/j.neuint.2011.05.015

    Article  CAS  PubMed  Google Scholar 

  • Lu Z (2011) Physiology of the ear and brain: how fish hear. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Academic, San Diego, pp 292–297

    Chapter  Google Scholar 

  • Lynch KS, Ball GF (2008) Noradrenergic deficits alter processing of communication signals in female songbirds. Brain Behav Evol 72(3):207–214. doi:10.1159/000157357

    Article  PubMed  Google Scholar 

  • Ma PM (1994) Catecholaminergic systems in the zebrafish. II. Projection pathways and pattern of termination of the locus coeruleus. J Comp Neurol 344(2):256–269. doi:10.1002/cne.903440207

    Article  CAS  PubMed  Google Scholar 

  • Maison SF, Liu XP, Eatock RA, Sibley DR, Grandy DK, Liberman MC (2012) Dopaminergic signaling in the cochlea: receptor expression patterns and deletion phenotypes. J Neurosci 32(1):344–355. doi:10.1523/JNEUROSCI.4720-11.2012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maney DL (2013) The incentive salience of courtship vocalizations: hormone-mediated ‘wanting’ in the auditory system. Hear Res 305:19–30. doi:10.1016/j.heares.2013.04.011

    Article  CAS  PubMed  Google Scholar 

  • Maney DL, Pinaud R (2011) Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front Neuroendocrinol 32(3):287–302. doi:10.1016/j.yfrne.2010.12.002

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCormick CA (1999) Anatomy of the central auditory pathways of fish and amphibians. In: Popper A, Fay RR (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 155–217

    Chapter  Google Scholar 

  • McCormick CA (2011) Auditory/lateral line CNS: anatomy. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Academic, San Diego, pp 283–291

    Chapter  Google Scholar 

  • McIver EL, Marchaterre MA, Rice AN, Bass AH (2014) Novel underwater soundscape: acoustic repertoire of plainfin midshipman fish. J Exp Biol 217:2377–2389. doi:10.1242/jeb.102772

    Article  PubMed  Google Scholar 

  • McKibben JR, Bass AH (1998) Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. J Acoust Soc Am 104(6):3520–3533

    Article  CAS  PubMed  Google Scholar 

  • McKibben JR, Bass AH (1999) Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: single tones. J Comp Physiol A 184(6):563–576

    Article  CAS  PubMed  Google Scholar 

  • McKibben JR, Bass AH (2001a) Effects of temporal envelope modulation on acoustic signal recognition in a vocal fish, the plainfin midshipman. J Acoust Soc Am 109(6):2934–2943

    Article  CAS  PubMed  Google Scholar 

  • McKibben JR, Bass AH (2001b) Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: harmonic and beat stimuli. J Comp Physiol A 187(4):271–285

    Article  CAS  PubMed  Google Scholar 

  • Mello CV, Pinaud R, Ribeiro S (1998) Noradrenergic system of the zebra finch brain: immunocytochemical study of dopamine-beta-hydroxylase. J Comp Neurol 400(2):207–228. doi:10.1002/(SICI)1096-9861(19981019)400:2<207::AID-CNE4>3.0.CO;2-D

    Google Scholar 

  • Niu X, Canlon B (2006) The signal transduction pathway for the dopamine D1 receptor in the guinea-pig cochlea. Neuroscience 137(3):981–990. doi:10.1016/j.neuroscience.2005.10.044

    Article  CAS  PubMed  Google Scholar 

  • O’Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519(18):3599–3639. doi:10.1002/cne.22735

    Article  PubMed  Google Scholar 

  • O’Connell LA, Hofmann HA (2012) Evolution of a vertebrate social decision-making network. Science 336(6085):1154–1157. doi:10.1126/science.1218889

    Article  PubMed  CAS  Google Scholar 

  • O’Connell LA, Fontenot MR, Hofmann HA (2011) Characterization of the dopaminergic system in the brain of an African cichlid fish, Astatotilapia burtoni. J Comp Neurol 519(1):75–92. doi:10.1002/cne.22506

    Article  PubMed  CAS  Google Scholar 

  • Pasqualini C, Weltzien FA, Vidal B, Baloche S, Rouget C, Gilles N, Servent D, Vernier P, Dufour S (2009) Two distinct dopamine D2 receptor genes in the European eel: molecular characterization, tissue-specific transcription, and regulation by sex steroids. Endocrinology 150(3):1377–1392. doi:10.1210/en.2008-0578

    Article  CAS  PubMed  Google Scholar 

  • Pawlisch BA, Stevenson SA, Riters LV (2011) alpha(1)-Noradrenegic receptor antagonism disrupts female songbird responses to male song. Neurosci Lett 496(1):20–24. doi:10.1016/j.neulet.2011.03.078

    Article  CAS  PubMed  Google Scholar 

  • Petersen CL, Timothy M, Kim DS, Bhandiwad AA, Mohr RA, Sisneros JA, Forlano PM (2013) Exposure to advertisement calls of reproductive competitors activates vocal-acoustic and catecholaminergic neurons in the plainfin midshipman fish, Porichthys notatus. PLoS One 8(8), e70474. doi:10.1371/journal.pone.0070474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Puzdrowski RL (1989) Peripheral distribution and central projections of the lateral-line nerves in goldfish, Carassius auratus. Brain Behav Evol 34(2):110–131

    Article  CAS  PubMed  Google Scholar 

  • Remage-Healey L, Bass AH (2004) Rapid, hierarchical modulation of vocal patterning by steroid hormones. J Neurosci 24(26):5892–5900

    Article  CAS  PubMed  Google Scholar 

  • Remage-Healey L, Bass AH (2005) Rapid elevations in both steroid hormones and vocal signaling during playback challenge: a field experiment in Gulf toadfish. Horm Behav 47(3):297–305

    Article  CAS  PubMed  Google Scholar 

  • Rink E, Wullimann MF (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889(1-2):316–330

    Article  CAS  PubMed  Google Scholar 

  • Rink E, Wullimann MF (2002) Connections of the ventral telencephalon and tyrosine hydroxylase distribution in the zebrafish brain (Danio rerio) lead to identification of an ascending dopaminergic system in a teleost. Brain Res Bull 57(3-4):385–387

    Article  CAS  PubMed  Google Scholar 

  • Riters LV (2012) The role of motivation and reward neural systems in vocal communication in songbirds. Front Neuroendocrinol 33(2):194–209. doi:10.1016/j.yfrne.2012.04.002

    Article  PubMed Central  PubMed  Google Scholar 

  • Roberts BL, Meredith GE, Maslam S (1989) Immunocytochemical analysis of the dopamine system in the brain and spinal cord of the European eel, Anguilla anguilla. Anat Embryol (Berl) 180(4):401–412

    Article  CAS  Google Scholar 

  • Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York

    Google Scholar 

  • Rohmann KN, Bass AH (2011) Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish. J Exp Biol 214(Pt 11):1931–1942. doi:10.1242/jeb.054114

    Article  PubMed Central  PubMed  Google Scholar 

  • Rohmann KN, Deitcher DL, Bass AH (2009) Calcium-activated potassium (BK) channels are encoded by duplicate slo1 genes in teleost fishes. Mol Biol Evol 26(7):1509–1521. doi:10.1093/molbev/msp060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rohmann KN, Fergus DJ, Bass AH (2013) Plasticity in ion channel expression underlies variation in hearing during reproductive cycles. Curr Biol 23(8):678–683. doi:10.1016/j.cub.2013.03.014

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rountree RA, Perkins PJ, Kenney RD, Hinga KR (2002) Sounds of Western North Atlantic Fishes: Data rescue. Bioacoustics 12:242–244

    Article  Google Scholar 

  • Ruel J, Nouvian R, Gervais d’Aldin C, Pujol R, Eybalin M, Puel JL (2001) Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur J Neurosci 14(6):977–986. pii: ejn1721

    Google Scholar 

  • Ruel J, Wang J, Rebillard G, Eybalin M, Lloyd R, Pujol R, Puel JL (2007) Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res 227(1-2):19–27. doi:10.1016/j.heares.2006.08.017

    Article  CAS  PubMed  Google Scholar 

  • Ryu S, Holzschuh J, Mahler J, Driever W (2006) Genetic analysis of dopaminergic system development in zebrafish. J Neural Transm Suppl 70:61–66

    Article  CAS  PubMed  Google Scholar 

  • Sas E, Maler L, Tinner B (1990) Catecholaminergic systems in the brain of a gymnotiform teleost fish: an immunohistochemical study. J Comp Neurol 292(1):127–162. doi:10.1002/cne.902920109

    Article  CAS  PubMed  Google Scholar 

  • Schall U, Keysers C, Kast B (1999) Pharmacology of sensory gating in the ascending auditory system of the pigeon (Columba livia). Psychopharmacology (Berl) 145(3):273–282

    Article  CAS  Google Scholar 

  • Sisneros JA (2009a) Seasonal plasticity of auditory saccular sensitivity in the vocal plainfin midshipman fish, Porichthys notatus. J Neurophysiol 102(2):1121–1131. doi:10.1152/jn.00236.2009

    Article  PubMed  Google Scholar 

  • Sisneros JA (2009b) Steroid-dependent auditory plasticity for the enhancement of acoustic communication: recent insights from a vocal teleost fish. Hear Res 252(1-2):9–14. doi:10.1016/j.heares.2008.12.007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sisneros JA, Bass AH (2003) Seasonal plasticity of peripheral auditory frequency sensitivity. J Neurosci 23(3):1049–1058

    CAS  PubMed  Google Scholar 

  • Sisneros JA, Marchaterre MA, Bass AH (2002) Otolithic endorgan projections of the inner ear in a vocal fish. Bioacoustics 12:137–139

    Article  Google Scholar 

  • Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004a) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305(5682):404–407

    Article  CAS  PubMed  Google Scholar 

  • Sisneros JA, Forlano PM, Knapp R, Bass AH (2004b) Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen Comp Endocrinol 136(1):101–116

    Article  CAS  PubMed  Google Scholar 

  • Sisneros JA, Alderks PW, Leon K, Sniffen B (2009) Morphometric changes associated with the reproductive cycle and behaviour of the intertidal-nesting, male plainfin midshipman Porichthys notatus. J Fish Biol 74(1):18–36. doi:10.1111/j.1095-8649.2008.02104.x

    Article  CAS  PubMed  Google Scholar 

  • Smith DW, Keil A (2015) The biological role of the medial olivocochlear efferents in hearing: separating evolved function from exaptation. Front Syst Neurosci 9:12. doi:10.3389/fnsys.2015.00012

    PubMed Central  PubMed  Google Scholar 

  • Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W (2011) Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. Nat Commun 2:171. doi:10.1038/ncomms1171

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tomchik SM, Lu ZM (2006) Modulation of auditory signal-to-noise ratios by efferent stimulation. J Neurophysiol 95(6):3562–3570

    Article  PubMed Central  PubMed  Google Scholar 

  • Vacher C, Pellegrini E, Anglade I, Ferriere F, Saligaut C, Kah O (2003) Distribution of dopamine D-2 receptor mRNAs in the brain and the pituitary of female rainbow trout: an in situ hybridization study. J Comp Neurol 458(1):32–45

    Article  CAS  PubMed  Google Scholar 

  • Valdes-Baizabal C, Soto E, Vega R (2015) Dopaminergic modulation of the voltage-gated sodium current in the cochlear afferent neurons of the rat. PLoS One 10(3), e0120808. doi:10.1371/journal.pone.0120808

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Velho TA, Lu K, Ribeiro S, Pinaud R, Vicario D, Mello CV (2012) Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds. PLoS One 7(5), e36276. doi:10.1371/journal.pone.0036276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vetillard A, Benanni S, Saligaut C, Jego P, Bailhache T (2002) Localization of tyrosine hydroxylase and its messenger RNA in the brain of rainbow trout by immunocytochemistry and in situ hybridization. J Comp Neurol 449(4):374–389

    Article  CAS  PubMed  Google Scholar 

  • Weeg MS, Bass AH (2000) Central lateral line pathways in a vocalizing fish. J Comp Neurol 418(1):41–64

    Article  CAS  PubMed  Google Scholar 

  • Weeg MS, Bass AH (2002) Frequency response properties of lateral line superficial neuromasts in a vocal fish, with evidence for acoustic sensitivity. J Neurophysiol 88(3):1252–1262

    PubMed  Google Scholar 

  • Weeg MS, Land BR, Bass AH (2005) Vocal pathways modulate efferent neurons to the inner ear and lateral line. J Neurosci 25(25):5967–5974

    Article  CAS  PubMed  Google Scholar 

  • Zeddies DG, Fay RR, Alderks PW, Shaub KS, Sisneros JA (2010) Sound source localization by the plainfin midshipman fish, Porichthys notatus. J Acoust Soc Am 127(5):3104–3113. doi:10.1121/1.3365261

    Article  PubMed  Google Scholar 

  • Zeddies DG, Fay RR, Gray MD, Alderks PW, Acob A, Sisneros JA (2012) Local acoustic particle motion guides sound-source localization behavior in the plainfin midshipman fish, Porichthys notatus. J Exp Biol 215(Pt 1):152–160. doi:10.1242/jeb.064998

    Article  PubMed  Google Scholar 

  • Zikopoulos B, Dermon CR (2005) Comparative anatomy of alpha(2) and beta adrenoceptors in the adult and developing brain of the marine teleost the red porgy (Pagrus pagrus, Sparidae): [(3)H]clonidine and [(3)H]dihydroalprenolol quantitative autoradiography and receptor subtypes immunohistochemistry. J Comp Neurol 489(2):217–240. doi:10.1002/cne.20641

    Article  CAS  PubMed  Google Scholar 

  • Zottoli SJ, Van Horne C (1983) Posterior lateral line afferent and efferent pathways within the central nervous system of the goldfish with special reference to the Mauthner cell. J Comp Neurol 219(1):100–111. doi:10.1002/cne.902190110

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

In terms of producing numerous foundational studies of fish auditory end organs at the morphological and functional level, Art Popper is truly a pioneer and set the groundwork for many of us interested in fish hearing. Work from Art’s lab is inspirational in terms of scope and diversity of species that have been studied. PMF had the pleasure of getting to know Dick Fay personally during a summer spent at the Marine Biological Laboratory in Woods Hole, MA while collaborating with him and JAS. Dick’s insights and contributions into the physiology, anatomy and behavior of hearing in fishes cannot be overstated. It was an honor to work with and learn from him on a daily basis as Dick is exemplary in his patience, kindness, and generosity on a scientific and personal level.

Although JAS never had the opportunity to work with Art Popper, JAS has been greatly influenced by Art’s research and career, and recently JAS has had to pleasure of co-organizing a major conference on the effects of noise on fish and aquatic life which has been a great experience. Art has been a great mentor and very generous with his time as he truly cares for the next generation of fish bioacoustic scientists. Dick Fay has always been a “gentlemen” scientist and JAS has been the fortunate recipient of his mentorship during a critical period of JAS’s pre-tenure career. JAS is truly grateful for his friendship, advice, and great many discussions of fish hearing and auditory physiology.

We thank the numerous students from both the Forlano and Sisneros lab that contributed to studies described here, Midge Marchaterre for assistance with animal collections and Jonathan Perelmuter for help with figure 7. We also thank Carol Vines, Gary Cherr, Kitty Brown, and staff at the Bodega Marine Laboratory and Rob Dickie of AREAC, Brooklyn College for logistical support. This work was supported by NIH SC2DA034996 to PMF, National Science Foundation IOS-0642214 to JAS, PSC-CUNY Awards 64519-00 42 and 65650-00 43 jointly funded by The Professional Staff Congress and The City University of New York to PMF, Leonard and Claire Tow Travel Award to PMF and Brooklyn College and CUNY Research Foundation. Work conducted at the Marine Biological Laboratory, Woods Hole, MA was partially supported by MBL Faculty Research Fellowships to PMF and JAS.

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Authors and Affiliations

  1. Department of Biology, Brooklyn College, and The Graduate Center, City University of New York, Brooklyn, NY, USA

    Paul M. Forlano

  2. Aquatic Research and Environmental Assessment Center, Brooklyn College, Brooklyn, NY, USA

    Paul M. Forlano

  3. Departments of Psychology and Biology, University of Washington, Seattle, WA, USA

    Joseph A. Sisneros

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  1. Paul M. Forlano
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  2. Joseph A. Sisneros
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Correspondence to Paul M. Forlano .

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  1. Department of Psychology, University of Washington, Seattle, Washington, USA

    Joseph A. Sisneros

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Forlano, P.M., Sisneros, J.A. (2016). Neuroanatomical Evidence for Catecholamines as Modulators of Audition and Acoustic Behavior in a Vocal Teleost. In: Sisneros, J. (eds) Fish Hearing and Bioacoustics. Advances in Experimental Medicine and Biology, vol 877. Springer, Cham. https://doi.org/10.1007/978-3-319-21059-9_19

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