Abstract
Among fishes, acoustic communication is best studied in toadfishes, a single order and family that includes species commonly known as toadfish and midshipman. However, there is a lack of comparative anatomical and physiological studies, making it difficult to identify both shared and derived mechanisms of vocalization among toadfishes. Here, vocal nerve labeling and intracellular in vivo recording and staining delineated the hindbrain vocal network of the Gulf toadfish Opsanus beta. Dextran-biotin labeling of the vocal nerve or intracellular neurobiotin fills of motoneurons delineated a midline vocal motor nucleus (VMN). Motoneurons showed bilaterally extensive dendritic arbors both within and lateral to the paired motor nuclei. The motoneuron activity matched that of the spike-like vocal nerve motor volley that determines the natural call duration and frequency. Ipsilateral vocal nerve labeling with biocytin or neurobiotin yielded dense bilateral transneuronal filling of motoneurons and coextensive columns of premotor neurons. These premotor neurons generated pacemaker-like action potentials matched 1:1 with vocal nerve and motoneuron firing. Transneuronal transport further revealed connectivity within and between the pacemaker-motor circuit and a rostral prepacemaker nucleus. Unlike the pacemaker-motor circuit, prepacemaker firing did not match the frequency of vocal nerve activity but instead was predictive of the duration of the vocal nerve volley that codes for call duration. Transneuronally labeled terminal-like boutons also occurred in auditory-recipient hindbrain nuclei, including neurons innervating the inner ear and lateral line organs. Together with studies of midshipman, we propose that separate premotor populations coding vocal frequency and duration with direct premotor coupling to auditory-lateral line nuclei are plesiomorphic characters for toadfishes. Unlike in midshipman, transneuronal labeling in toadfishes reveals an expansive column of pacemaker neurons that is weakly coupled to prepacemaker neurons, a character that likely depends on the extent of gap junction coupling. We propose that these and other anatomical characters contribute to neurophysiological properties that, in turn, sculpt the species-typical patterning of frequency and amplitude-modulated vocalizations.
References
1.
Amorim MCP (2006): Diversity in sound production in fish; in Ladich F, Collin SP, Moller P, Kapoor BG (eds): Communication in Fishes. Enfield, Science, vol 1, pp 71-106.
2.
Arriaga G, Zhou EP, Jarvis ED (2012): Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One 7:e46610.
3.
Bass AH (1989): Evolution of vertebrate motor systems for acoustic and electric communication: peripheral and central elements. Brain Behav Evol 33:237-247.
4.
Bass AH, Andersen K (1991): Intra- and intersexual dimorphisms in the sound generating motor system in a vocalizing fish: motor axon number and size. Brain Behav Evol 37:204-214.
5.
Bass AH, Baker R (1990): Sexual dimorphisms in the vocal control system of a teleost fish: morphology of physiologically identified neurons. J Neurobiol 21:1155-1168.
6.
Bass AH, Baker R (1991): Evolution of homologous traits. Brain Behav Evol 38:240-254.
7.
Bass AH, Baker R (1997): Phenotypic specification of hindbrain rhombomeres and the origins of rhythmic circuits in vertebrates. Brain Behav Evol 50:3-16.
8.
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. Cambridge, MIT Press, pp 493-514.
9.
Bass AH, Bodnar DA, Marchaterre MA (2000): Midbrain acoustic circuitry in a vocalizing fish. J Comp Neurol 419:505-531.
10.
Bass AH, Bodnar DA, Marchaterre MA (2001): Acoustic nuclei in the medulla and midbrain of the vocalizing Gulf toadfish (Opsanus beta). Brain Behav Evol 57:63-79.
11.
Bass AH, Chagnaud BP (2012): Shared developmental and evolutionary origins for neural basis of vocal-acoustic and pectoral-gestural signaling. Proc Natl Acad Sci USA 109:10677-10684.
12.
Bass AH, Chagnaud BP, Feng N (in press): Comparative neurobiology of sound production in fishes; in Ladich F (ed): Sound Communication in Fishes. Berlin, Springer.
13.
Bass AH, Gilland EH, Baker R (2008): Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment. Science 321:417-421.
14.
Bass AH, Horvath BJ, Brothers EB (1996): Nonsequential developmental trajectories lead to dimorphic vocal circuitry for males with alternative reproductive tactics. J Neurobiol 30:493-504.
15.
Bass AH, Ladich F (2008): Vocal-acoustic communication: from neurons to behavior; in Webb JF, Fay RR, Popper AN (eds): Fish Bioacoustics. Berlin, Springer, pp 253-278.
16.
Bass AH, Marchaterre MA, Baker R (1994): Vocal-acoustic pathways in a teleost fish. J Neurosci 14:4025-4039.
17.
Bennett MVL, Crain SM, Grundfest H (1959): Electrophysiology of supramedullary neurons in Spheroides maculatus. 1. Orthodromic and antidromic responses. J Gen Physiol 43:159-188.
18.
Bennett MVL, Pappas GD (1965): Neurophysiology and ultrastructure of a synchronously firing nucleus in toadfish, Opsanus. Fed Proc 24:462.
19.
Bennett NT, Weiser M, Baker R, Bennett MVL (1985): Toadfish sonic motor system. 1. Physiology. Bio Bull 169:546.
20.
Boyle KS, Dewan AK, Tricas TC (2013): Fast drum strokes: novel and convergent features of sonic muscle ultrastructure, innervation, and motor neuron organization in the pyramid butterflyfish (Hemitaurichthys polylepis). J Morphol 274:377-394.
21.
Bradbury J, Vehrencamp S (2011): Principles of animal communication. Sunderland, Sinauer.
22.
Brantley RK, Bass AH (1994): Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish, Porichthys notatus (Teleostei, Batrachoididae). Ethology 96:213-232.
23.
Brantley RK, Tseng J, Bass AH (1993): The ontogeny of inter- and intrasexual vocal muscle dimorphisms in a sound-producing fish. Brain Behav Evol 42:336-349.
24.
Carlson BA, Bass AH (2000): Sonic/vocal motor pathways in squirrelfish (Teleostei, Holocentridae). Brain Behav Evol 56:14-28.
25.
Chagnaud BP, Bass AH (2013): Vocal corollary discharge communicates call duration to vertebrate auditory system. J Neurosci 33:18775-11878.
26.
Chagnaud BP, Baker R, Bass AH (2011): Vocalization frequency and duration are coded in separate hindbrain nuclei. Nat Commun 2:346.
27.
Chagnaud BP, Zee MC, Baker R, Bass AH (2012): Innovations in motoneuron synchrony drive rapid temporal modulations in vertebrate acoustic signaling. J Neurophysiol 107:3528-3542.
28.
Cohen MJ, Winn HE (1967): Electrophysiological observations on hearing and sound production in the fish, Porichthys notatus. J Exp Zool 165:355-369.
29.
Demski LS, Gerald JW (1972): Sound production evoked by electrical stimulation of the brain in toadfish (Opsanus beta). Anim Behav 20:507-513.
30.
Demski LS, Gerald JW (1974): Sound production and other behavioral effects of midbrain stimulation in free-swimming toadfish, Opsanus beta. Brain Behav Evol 9:41-59.
31.
Demski LS, Gerald JW, Popper AN (1973): Central and peripheral mechanisms of teleost sound production. Am Zool 13:1141-1167.
32.
Edds-Walton PL, Mangiamele LA, Rome LC (2002): Variations of pulse repetition rate in boatwhistle sounds from oyster toadfish, Opsanus tau, around Waquoit bay, Massachusetts. Bioacoustics 13:153-173.
33.
Elemans CPH, Mead AF, Rome LC, Goller F (2008): Superfast vocal muscles control song production in songbirds. PLoS One 3:e2581.
34.
Fine M, Economos D, Radtke R, McClung J (1984): Ontogeny and sexual dimorphism of motor nucleus in the oyster toadfish. J Comp Neurol 255:105-110.
35.
Fine ML, Thorson RF (2008): Use of passive acoustics for assessing behavioral interactions in individual toadfish. Trans Am Fish Soc 137:627-637.
36.
Fish MP, Mowbray WH (1970): Sounds of Western North Atlantic fishes. Baltimore, Johns Hopkins Press.
37.
Funakoshi K, Abe T, Kishida R (1995): Trigeminal, vagal, and spinal projections of supramedullary cells in the puffer fish, Takifugu niphobles. J Comp Neurol 358:552-562.
38.
Funakoshi K, Kadota T, Atobe Y, Nakano M, Goris RC, Kishida R (1998): Gastrin/CCK-ergic innervation of cutaneous mucous gland by the supramedullary cells of the puffer fish Takifugu niphobles. Neurosci Lett 258:171-174.
39.
Goodson JL, Bass AH (2000a): Vasotocin innervation and modulation of vocal-acoustic circuitry in the teleost Porichthys notatus. J Comp Neurol 422:363-379.
40.
Goodson JL, Bass AH (2000b): Rhythmic midbrain-evoked vocalization is inhibited by vasoactive intestinal polypeptide in the teleost Porichthys notatus. Brain Res 865:107-111.
41.
Goodson JL, Bass AH (2000c): Forebrain peptides modulate sexually polymorphic vocal circuitry. Nature 403:769-772.
42.
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 448:298-322.
43.
Greenfield DW, Winterbottom R, Collette BB (2008): Review of the toadfish genera (Teleostei: Batrachoididae). Proc Calif Acad Sci 59:665-710.
44.
Highstein SM (1992): The efferent control of the organs of balance and equilibrium in the toadfish, Opsanus tau. Ann NY Acad Sci 656:108-123.
45.
Highstein SM, Baker R (1986): Organization of the efferent, vestibular nuclei and nerves of the toadfish, Opsanus tau. J Comp Neurol 243:309-325.
46.
Ibara RM, Penny LT, Ebeling AW, van Dykhuizen G, Cailliet G (1983): The mating call of the plainfin midshipman fish, Porichthys notatus; in Noakes DLG, Lindquist DG, Helfman GS, Ward JA (eds): Predators and Prey in Fishes. The Hague, Junk, pp 205-212.
47.
Jarvis ED, Ribeiro S, da Silva ML, Ventura D, Vielliard J, Mello CV (2000): Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406:628-632.
48.
Kittelberger JM, Land BR, Bass AH (2006): Midbrain periaqueductal gray and vocal patterning in a teleost fish. J Neurophysiol 96:71-85.
49.
Knapp R, Marchaterre MA, Bass AH (1999): Early development of the motor and premotor circuitry of a sexually dimorphic vocal pathway in a teleost fish. J Neurobiol 38:475-490.
50.
Ladich F, Bass AH (1996): Sonic/vocal-acousticolateralis pathways in teleost fishes: a transneuronal biocytin study in mochokid catfish. J Comp Neurol 374:493-505.
51.
Ladich F, Fine ML (2006): Sound-generating mechanisms in fishes: a unique diversity in vertebrates; in Ladich F, Collin SP, Moller P, Kapoor BG (eds): Communication in Fishes. Enfield, Science, vol 1, pp 3-43.
52.
Leininger EC, Kelley DB (2013): Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls. Proc Biol Sci 280;20122639.
53.
Maruska K, Mensinger A (2009): Acoustic characteristics and variations in grunt vocalizations in the oyster toadfish Opsanus tau. Environ Biol Fish 84:325-337.
54.
McIver E, Marchaterre M, Rice A, Bass A (2014): Novel underwater soundscape: acoustic repertoire of plainfin midshipman fish. J Exp Biol 2014;217:2377-2389.
55.
Mosharo K, Lobel P (2012): Acoustic signals of two toadfishes from Belize: Sanopus astrifer and Batrachoides gilberti (Batrachoididae). Environ Biol Fish 94:623-638.
56.
Nowicki S, Westneat M, Hoese W (1992): Birdsong: motor function and the evolution of communication. Semin Neurosci 4:385-390.
57.
Onuki A, Somiya H (2007): Innervation of sonic muscles in teleosts: occipital versus spinal nerves. Brain Behav Evol 69:132-141.
58.
Pappas G, Bennett M (1966): Specialized junctions involved in electrical transmission between neurons. Ann NY Acad Sci 137:495-508.
59.
Radtke R, Fine M, Bell J (1995): Somatic and otolith growth in the oyster toadfish (Opsanus tau L.). J Exp Mar Biol Ecol 90:259-275.
60.
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 47:297-305.
61.
Remage-Healey LH, Bass AH (2006): From social behavior to neurons: rapid modulation of advertisement calling and vocal pattern generators by steroid hormones. Horm Behav 50:432-441.
62.
Remage-Healey L, Nowacek DP, Bass AH (2006): Dolphin foraging sounds suppress calling and elevate stress hormone levels in a prey species, the Gulf toadfish. J Exp Biol 209:4444-4451.
63.
Rice AN, Bass AH (2009): Novel vocal repertoire and paired swim bladders of the three-spined toadfish, Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae. J Exp Biol 212:1377-1391.
64.
Skoglund CR (1961): Functional analysis of swim-bladder muscles engaged in sound production of the toadfish. J Biophys Biochem Cytol 10:187-200.
65.
Striedter GF (1994): The vocal control pathways in budgerigars differ from those in songbirds. J Comp Neurol 343:35-56.
66.
Suthers R, Goller F, Pytte C (1999): The neuromuscular control of birdsong. Philos Trans R Soc Lond B Biol Sci 354:927-939.
67.
Tavolga WN (1958): Underwater sounds produced by two species of toadfish, Opsanus tau and Opsanus beta. Bull Mar Sci 8:278-284.
68.
Thorson RF, Fine ML (2002): Crepuscular changes in emission rate and parameters of the boatwhistle advertisement call of the Gulf toadfish, Opsanus beta. Environ Biol Fish 63:321-331.
69.
Walsh PW, Mommsen TP, Bass AH (1995): Biochemical and molecular aspects of singing in batrachoidid fishes; in Hochachka PW, Mommsen TP (eds): Biochemistry and Molecular Biology of Fishes. Amsterdam, Pergamon Press, vol 4, pp 279-289.
70.
Weeg MS, Land BR, Bass AH (2005): Vocal pathways modulate efferent neurons to the inner ear and lateral line. J Neurosci 25:5967-5974.
71.
Weiser M, Bennett NT, Bennett MVL, Baker R (1985): Toadfish sonic motor system. 2. Morphology. Biol Bull 169:556-557.
72.
Yager DD (1992): Underwater acoustic communication in the African pipid frog Xenopus borealis. Bioacoustics 4:1-24.
73.
Zornik E, Kelley DB (2008): Regulation of respiratory and vocal motor pools in the isolated brain of Xenopus laevis. J Neurosci 28:612-621.
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2014
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