Skip to main content
SpringerLink
Log in

Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Homologues of a neuron that contributes to a species-specific behavior were identified and characterized in species lacking that behavior. The nudibranch Tritonia diomedea swims by flexing its body dorsally and ventrally. The dorsal swim interneurons (DSIs) are components of the central pattern generator (CPG) underlying this rhythmic motor pattern and also activate crawling. Homologues of the DSIs were identified in six nudibranchs that do not exhibit dorsal–ventral swimming: Tochuina tetraquetra, Melibe leonina, Dendronotus iris, D. frondosus, Armina californica, and Triopha catalinae. Homology was based upon shared features that distinguish the DSIs from all other neurons: (1) serotonin immunoreactivity, (2) location in the Cerebral serotonergic posterior (CeSP) cluster, and (3) axon projection to the contralateral pedal ganglion. The DSI homologues, named CeSP-A neurons, share additional features with the DSIs: irregular basal firing, synchronous inputs, electrical coupling, and reciprocal inhibition. Unlike the DSIs, the CeSP-A neurons were not rhythmically active in response to nerve stimulation. The CeSP-A neurons in Tochuina and Triopha also excited homologues of the Tritonia Pd5 neuron, a crawling efferent. Thus, the CeSP-A neurons and the DSIs may be part of a conserved network related to crawling that may have been co-opted into a rhythmic swim CPG in Tritonia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ASD:

Antiserum diluent

CeSP:

Cerebral serotonergic posterior

CPG:

Central pattern generator

DSI:

Dorsal swim interneuron

PBS:

Phosphate buffered saline

Pd5:

Pedal 5

PdN2:

Pedal nerve 2

PP:

Pedal–pedal connective

Tpep:

Tritonia pedal peptide

References

  • Arbas EA (1983a) Neural correlates of flight loss in a Mexican grasshopper, Barytettix psolus. I. Motor and sensory cells. J Comp Neurol 216:369–380

    CAS  Google Scholar 

  • Arbas EA (1983b) Neural correlates of flight loss in a Mexican grasshopper, Barytettix psolus. II. DCMD and TCG interneurons. J Comp Neurol 216:381–389

    CAS  Google Scholar 

  • Arbas EA, Meinertzhagen IA, Shaw SR (1991) Evolution in nervous systems. Annu Rev Neurosci 14:9–38

    PubMed  CAS  Google Scholar 

  • Arshavsky YI, Deliagina TG, Orlovsky GN, Panchin YV, Popova LB (1992) Interneurones mediating the escape reaction of the marine mollusc Clione limacina. J Exp Biol 164:307–314

    Google Scholar 

  • Audesirk G, McCaman RE, Willows AOD (1979) The role of serotonin in the control of pedal ciliary activity by identified neurons in Tritonia diomedea. Comp Biochem Physiol C 62:87–91

    Google Scholar 

  • Auerbach SB, Grover LM, Farley J (1989) Neurochemical and immunocytochemical studies of serotonin in the Hermissenda central nervous system. Brain Res Bull 22:353–361

    PubMed  CAS  Google Scholar 

  • Baltzley MJ (2006) Evolution and neurobiology of the neural circuitry underlying crawling in nudibranch molluscs. Ph. D. Dissertation. University of North Carolina, Chapel Hill, NC

  • Bass AH (1986) Evolution of a vertebrate communication and orientation organ. In: Bullock TH (eds) Electric organs revisited. Wiley, New York

    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 21:1155–1168

    PubMed  CAS  Google Scholar 

  • Bass AH, Baker R (1997) Phenotypic specification of hindbrain rhombomeres and the origins of rhythmic circuits in vertebrates. Brain Behav Evol 50:3–16

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Bebbington A, Hughes GM (1973) Locomotion in Aplysia (Gastropoda, Opisthobranchia). Proc Malacol Soc Lond 40:399–405

    Google Scholar 

  • Bergh R (1894) Reports on the dredging operations off the West Coast of Central America to the Galapagos, to the West Coast of Mexico, and in the Gulf of California, in charge of Alexander Agassiz, carried on by the U.S. Fish Commission Steamer “Albatross”, during 1891, Lieut. Commander Z.L. Tanner, U.S.N., Commanding. XIII. Die Opisthobranchien. Bull Mus Comp Zool 25:125–233

    Google Scholar 

  • Bullock TH (2000) Revisiting the concept of identifiable neurons. Brain Behav Evol 55:236–240

    PubMed  CAS  Google Scholar 

  • Buschbeck EK, Strausfeld NJ (1997) The relevance of neural architecture to visual performance: phylogenetic conservation and variation in dipteran visual systems. J Comp Neurol 383:282–304

    PubMed  CAS  Google Scholar 

  • Cain SD, Wang JH, Lohmann KJ (2006) Immunochemical and electrophysiological analyses of magnetically responsive neurons in the mollusc Tritonia diomedea. J Comp Physiol A 192:235–245

    Google Scholar 

  • Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford University Press, New York

    Google Scholar 

  • Chiang J-TA, Steciuk M, Shtonda B, Avery L (2006) Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes. J Exp Biol 209:1859–1873

    PubMed  Google Scholar 

  • Comer CM, Robertson RM (2001) Identified nerve cells and insect behavior. Prog Neurobiol 63:409–439

    PubMed  CAS  Google Scholar 

  • Croll RP (1987) Distribution of monoamines in the central nervous system of the nudibranch gastropod, Hermissenda crassicornis. Brain Res 405:337–347

    PubMed  CAS  Google Scholar 

  • Croll RP, Boudko DY, Hadfield MG (2001) Histochemical survey of transmitters in the central ganglia of the gastropod mollusc Phestilla sibogae. Cell Tissue Res 305:417–432

    PubMed  CAS  Google Scholar 

  • Dorsett DA, Willows AOD, Hoyle G (1969) Centrally generated nerve impulse sequences determining swimming behaviour in Tritonia. Nature 224:711–712

    Google Scholar 

  • Dye JC, Meyer JH (1986) Central control of the electric organ discharge in weakly electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York

    Google Scholar 

  • Faulkes Z (2004) Loss of escape responses and giant neurons in the tailflipping circuits of slipper lobsters, Ibacus spp. (Decapoda, Palinura, Scyllaridae). Arthropod Struct Dev 33:113–123

    PubMed  Google Scholar 

  • Fickbohm DJ, Katz PS (2000) Paradoxical actions of the serotonin precursor 5-hydroxytryptophan on the activity of identified serotonergic neurons in a simple motor circuit. J Neurosci 20:1622–1634

    PubMed  CAS  Google Scholar 

  • Fickbohm DJ, Lynn-Bullock CP, Spitzer N, Caldwell HK, Katz PS (2001) Localization and quantification of 5-hydroxytryptophan and serotonin in the central nervous systems of Tritonia and Aplysia. J Comp Neurol 437:91–105

    PubMed  CAS  Google Scholar 

  • Fredman SM, Jahan-Parwar B (1983) Command neurons for locomotion in Aplysia. J Neurophysiol 49:1092–1117

    PubMed  CAS  Google Scholar 

  • Frost WN, Hoppe TA, Wang J, Tian LM (2001) Swim initiation neurons in Tritonia diomedea. Am Zool 41:952–961

    Google Scholar 

  • Gamkrelidze GN, Laurienti PJ, Blankenship JE (1995) Identification and characterization of cerebral ganglion neurons that induce swimming and modulate swim-related pedal ganglion neurons in Aplysia brasiliana. J Neurophysiol 74:1444–1462

    PubMed  CAS  Google Scholar 

  • Getting PA (1981) Mechanisms of pattern generation underlying swimming in Tritonia. I. Neuronal network formed by monosynaptic connections. J Neurophysiol 46:65–79

    PubMed  CAS  Google Scholar 

  • Getting PA (1983) Mechanisms of pattern generation underlying swimming in Tritonia. II. Intrinsic and synaptic mechanisms for delayed excitation. J Neurophysiol 49:1036–1050

    PubMed  CAS  Google Scholar 

  • Getting PA, Dekin MS (1985) Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator. J Neurophysiol 53:466–480

    PubMed  CAS  Google Scholar 

  • Getting PA, Lennard PR, Hume RI (1980) Central pattern generator mediating swimming in Tritonia. I. Identification and synaptic interactions. J Neurophysiol 44:151–164

    PubMed  CAS  Google Scholar 

  • Goslow GE, Dial KP, Jenkins FA (1989) The avian shoulder: an experimental approach. Am Zool 29:287–301

    Google Scholar 

  • Grande C, Templado J, Cervera JL, Zardoya R (2004) Phylogenetic relationships among Opisthobranchia (Mollusca: Gastropoda) based on mitochondrial cox 1, trn V, and rrnL genes. Mol Phylogen Evol 33:378–388

    CAS  Google Scholar 

  • Grant K, Bell CC, Clausse S, Ravaille M (1986) Morphology and physiology of the brainstem nuclei controlling the electric organ discharge in mormyrid fish. J Comp Neurol 245:514–530

    PubMed  CAS  Google Scholar 

  • Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14:39–57

    PubMed  CAS  Google Scholar 

  • Herrel A, Meyers JJ, Nishikawa KC, De Vree F (2001) The evolution of feeding motor patterns in lizards: modulatory complexity and possible constraints. Am Zool 41:1311–1320

    Google Scholar 

  • Hume RI, Getting PA (1982) Motor organization of Tritonia swimming. II. Synaptic drive to flexion neurons from premotor interneurons. J Neurophysiol 47:75–90

    PubMed  CAS  Google Scholar 

  • Hume RI, Getting PA, Del Beccaro MA (1982) Motor organization of Tritonia swimming. I. Quantitative analysis of swim behavior and flexion neuron firing patterns. J Neurophysiol 47:60–74

    PubMed  CAS  Google Scholar 

  • Jing J, Gillette R (1995) Neuronal elements that mediate escape swimming and suppress feeding behavior in the predatory sea slug Pleurobranchaea. J Neurophysiol 74:1900–1910

    PubMed  CAS  Google Scholar 

  • Jing J, Gillette R (1999) Central pattern generator for escape swimming in the notaspid sea slug Pleurobranchaea californica. J Neurophysiol 81:654–667

    PubMed  CAS  Google Scholar 

  • Jing J, Gillette R (2000) Escape swim network interneurons have diverse roles in behavioral switching and putative arousal in Pleurobranchaea. J Neurophysiol 83:1346–1355

    PubMed  CAS  Google Scholar 

  • Jing J, Gillette R (2003) Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells. J Neurosci 23:3039–3051

    PubMed  CAS  Google Scholar 

  • Kabotyanskii EA, Sakharov DA (1991) Neuronal correlates of the serotonin-dependent behavior of the pteropod mollusc Clione limacina. Neurosci Behav Physiol 21:422–435

    PubMed  CAS  Google Scholar 

  • Katz PS (1991) Neuromodulation and the evolution of a simple motor system. Semin Neurosci 3:379–389

    Google Scholar 

  • Katz PS, Harris-Warrick RM (1999) The evolution of neuronal circuits underlying species-specific behavior. Curr Opin Neurobiol 9:628–633

    PubMed  CAS  Google Scholar 

  • Katz PS, Newcomb JM (2006) A Tale of Two CPGs: Phylogenetically polymorphic networks. In: Kaas J (eds) Evolution of nervous systems, vol 1, Theories, Development, Invertebrates, Elsevier, Oxford UK, pp 367–374

  • Katz PS, Tazaki K (1992) Comparative and evolutionary aspects of the crustacean stomatogastric system. In: Harris-Warrick RM, Marder E, Selverston AI, Moulins M (eds) Dynamic biological networks. MIT, Cambridge

    Google Scholar 

  • Katz PS, Getting PA, Frost WN (1994) Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367:729–731

    PubMed  CAS  Google Scholar 

  • Katz PS, Fickbohm DJ, Lynn-Bullock CP (2001) Evidence that the central pattern generator for swimming in Tritonia arose from a non-rhythmic neuromodulatory arousal system: implications for the evolution of specialized behavior. Am Zool 41:962–975

    Google Scholar 

  • Katz PS, Sakurai A, Clemens S, Davis D (2004) Cycle period of a network oscillator is independent of membrane potential and spiking activity in individual central pattern generator neurons. J Neurophysiol 92:1904–1917

    PubMed  Google Scholar 

  • Kavanau JL (1990) Conservative behavioral evolution, the neural substrate. Anim Behav 39:758–767

    Google Scholar 

  • Kiehn O, Hounsgaard J, Sillar KT (1997) Basic building blocks of vertebrate spinal central pattern generators. In: Stein PSG, Grillner S, Selverston A (eds) Neurons, networks and motor behavior. MIT, Cambridge

    Google Scholar 

  • Land PW, Crow T (1985) Serotonin immunoreactivity in the circumesophageal nervous system of Hermissenda crassicornis. Neurosci Lett 62:199–205

    PubMed  CAS  Google Scholar 

  • Langenbach GEJ, Van Eijden TMGJ (2001) Mammalian feeding motor patterns. Am Zool 41:1338–1351

    Google Scholar 

  • Lloyd PE, Phares GE, Phillips NE, Willows AOD (1996) Purification and sequencing of neuropeptides from identified neurons in the marine mollusc, Tritonia. Peptides 17:17–23

    PubMed  CAS  Google Scholar 

  • Longley RD, Longley AJ (1986) Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. J Neurobiol 17:339–358

    PubMed  CAS  Google Scholar 

  • Lucki I (1998) The spectrum of behaviors influenced by serotonin. Biol Psychiatry 44:151–162

    PubMed  CAS  Google Scholar 

  • Mackey SL, Carew TJ (1983) Locomotion in Aplysia: triggering by serotonin and bag cells extract. J Neurosci 3:1469–1477

    PubMed  CAS  Google Scholar 

  • Mackey SL, Kandel ER, Hawkins RD (1989) Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons. J Neurosci 9:4227–4235

    PubMed  CAS  Google Scholar 

  • Margoliash D, Fortune ES, Sutter ML, Yu AC, Wren-Hardin BD, Dave A (1994) Distributed representation in the song system of oscines: evolutionary implications and functional consequences. Brain Behav Evol 44:247–264

    PubMed  CAS  Google Scholar 

  • Marinesco S, Kolkman KE, Carew TJ (2004a) Serotonergic modulation in Aplysia. I. Distributed serotonergic network persistently activated by sensitizing stimuli. J Neurophysiol 92:2468–2486

    CAS  Google Scholar 

  • Marinesco S, Wickremasinghe N, Kolkman KE, Carew TJ (2004b) Serotonergic modulation in Aplysia. II. Cellular and behavioral consequences of increased serotonergic tone. J Neurophysiol 92:2487–2496

    CAS  Google Scholar 

  • McClellan AD, Brown GD, Getting PA (1994) Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin. J Comp Physiol A 174:257–266

    PubMed  CAS  Google Scholar 

  • McLean IW, Nakane PK (1974) Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083

    PubMed  CAS  Google Scholar 

  • McPherson D, Katz PS (2001) Identification of serotonergic cerebral neurons that project to the pedal ganglia of Aplysia californica. Program No. 943.10. Society for Neuroscience, Washington

  • Metzner W (1999) Neural circuitry for communication and jamming avoidance in gymnotiform electric fish. J Exp Biol 202:1365–1375

    PubMed  CAS  Google Scholar 

  • Newcomb JM, Katz PS (2003) Homologous serotonergic neurons in two molluscan species differentially participate in analogous locomotor behaviors. Program No. 403.7. Society for Neuroscience, Washington

  • Newcomb JM, Katz PS (2005) Evolution of central pattern generator circuitry in nudibranch molluscs: changes in the functions of identified neurons embedded in a common network. Program No. 752.2. Society for Neuroscience, Washington

  • Newcomb JM, Katz PS (2006) Patterns of neural evolution in nudibranch molluscs: functional divergence of homologous neurons embedded in a common neural network. Integr Comp Biol 45:1050

    Google Scholar 

  • Newcomb JM, Fickbohm DJ, Katz PS (2006) Comparative mapping of serotonin-immunoreactive neurons in the central nervous systems of nudibranch molluscs. J Comp Neurol 499:485–505

    PubMed  Google Scholar 

  • Nishikawa KC, Anderson CW, Deban SM, O’Reilly JC (1992) The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav Evol 40:125–140

    PubMed  CAS  Google Scholar 

  • Ono JK, McCaman RE (1984) Immunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia. Neurosci 11:549–560

    CAS  Google Scholar 

  • Palovcik RA, Basberg BA, Ram JL (1982) Behavioral state changes induced in Pleurobranchaea and Aplysia by serotonin. Behav Neural Biol 35:383–394

    PubMed  CAS  Google Scholar 

  • Panchin YV, Popova LB, Deliagina TG, Orlovsky GN, Arshavsky YI (1995) Control of locomotion in marine mollusk Clione limacina. VIII. Cerebropedal neurons. J Neurophysiol 73:1912–1923

    PubMed  CAS  Google Scholar 

  • Parsons DW, Pinsker HM (1989) Swimming in Aplysia brasiliana: behavioral and cellular effects of serotonin. J Neurophysiol 62:1163–1176

    PubMed  CAS  Google Scholar 

  • Paul DH (1991) Pedigrees of neurobehavioral circuits: tracing the evolution of novel behaviors by comparing motor patterns, muscles, and neurons in members of related taxa. Brain Behav Evol 38:226–239

    PubMed  CAS  Google Scholar 

  • Popescu IR, Willows AOD (1999) Sources of magnetic sensory input to identified neurons active during crawling in the marine mollusc Tritonia diomedea. J Exp Biol 202:3029–3036

    PubMed  Google Scholar 

  • Popescu IR, Frost WN (2002) Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22:1985–1993

    PubMed  CAS  Google Scholar 

  • Sakurai A, Katz PS (2003) Spike timing-dependent serotonergic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. J Neurosci 23:10745–10755

    PubMed  CAS  Google Scholar 

  • Sanderson SL (1988) Variation in neuromuscular activity during prey capture by trophic specialists and generalists (Pisces: Labridae). Brain Behav Evol 32:257–268

    PubMed  CAS  Google Scholar 

  • Satterlie RA, Norekian TP (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina III. Cerebral neurons. J Exp Biol 198:917–930

    PubMed  CAS  Google Scholar 

  • Satterlie RA, LaBarbera M, Spencer AN (1985) Swimming in the pteropod mollusc, Clione limacina I. Behaviour and morphology. J Exp Biol 116:189–204

    Google Scholar 

  • Schmidt RS (1992) Neural correlates of frog calling: production by two semi-independent generators. Behav Brain Res 50:17–30

    PubMed  CAS  Google Scholar 

  • Shaw SR, Meinertzhagen IA (1986) Evolutionary progression at synaptic connections made by identified homologous neurons. Proc Natl Acad Sci USA 83:7961–7965

    PubMed  CAS  Google Scholar 

  • Shaw SR, Moore D (1989) Evolutionary remodeling in a visual system through extensive changes in the synaptic connectivity of homologous neurons. Vis Neurosci 3:405–410

    Article  PubMed  CAS  Google Scholar 

  • Smith KK (1994) Are neuromotor systems conserved in evolution? Brain Behav Evol 43:293–305

    PubMed  CAS  Google Scholar 

  • Striedter GF (1994) The vocal control pathways in budgerigars differ from those in songbirds. J Comp Neurol 343:35–56

    PubMed  CAS  Google Scholar 

  • Striedter GF, Northcutt RG (1991) Biological hierarchies and the concept of homology. Brain Behav Evol 38:177–189

    PubMed  CAS  Google Scholar 

  • Sudlow LC, Jing J, Moroz LL, Gillette R (1998) Serotonin immunoreactivity in the central nervous system of the marine molluscs Pleurobranchaea californica and Tritonia diomedea. J Comp Neurol 395:466–480

    PubMed  CAS  Google Scholar 

  • Thollesson M (1999) Phylogenetic analysis of Euthyneura (Gastropoda) by means of the 16S rRNA gene: use of a ‘fast’ gene for ‘higher-level’ phylogenies. Proc R Soc Lond B 266:75–83

    Google Scholar 

  • Thompson S, Watson WH III (2005) Central pattern generator for swimming in Melibe. J Exp Biol 208:1347–1361

    PubMed  Google Scholar 

  • Thompson TE (1976) Biology of opisthobranch molluscs, vol. 1. Ray Society, London

  • Tian L-M, Kawai R, Crow T (2006) Serotonin-immunoreactive CPT interneurons in Hermissenda: identification of sensory input and motor projections. J Neurophysiol 96:327–335

    PubMed  CAS  Google Scholar 

  • Tierney AJ (1995) Evolutionary implications of neural circuit structure and function. Behav Processes 35:173–182

    Google Scholar 

  • von der Porten K, Parsons DW, Rothman BS, Pinsker H (1982) Swimming in Aplysia brasiliana: analysis of behavior and neuronal pathways. Behav Neural Biol 36:1–23

    PubMed  Google Scholar 

  • Vonnemann V, Schrödl M, Klussmann-Kolb A, Wägele H (2005) Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences. J Molluscan Stud 71:113–125

    Google Scholar 

  • Wägele H, Willan RC (2000) Phylogeny of the Nudibranchia. Zool J Linn Soc 130:83–181

    Google Scholar 

  • Wainwright PC (1989) Prey processing in Haemulid fishes: patterns of variation in pharyngeal jaw muscle activity. J Exp Biol 141:359–375

    Google Scholar 

  • Wainwright PC (2002) The evolution of feeding motor patterns in vertebrates. Curr Opin Neurobiol 12:691–695

    PubMed  CAS  Google Scholar 

  • Watson WH III, Newcomb JM, Thompson S (2002) Neural correlates of swimming behavior in Melibe leonina. Biol Bull 203:152–160

    PubMed  Google Scholar 

  • Weijs WA, Dantuma R (1994) Evolutionary approach to masticatory motor patterns in mammals. Adv Comp Environ Physiol 18:281–320

    Google Scholar 

  • Wiens BL, Brownell PH (1995) Neurotransmitter regulation of the heart in the nudibranch Archidoris montereyensis. J Neurophysiol 74:1639–1651

    PubMed  CAS  Google Scholar 

  • Wild JM (1994) The auditory–vocal–respiratory axis in birds. Brain Behav Evol 44:192–209

    PubMed  CAS  Google Scholar 

  • Wild JM (1997) Neural pathways for the control of birdsong production. J Neurobiol 33:653–670

    PubMed  CAS  Google Scholar 

  • Willows AOD (1967) Behavioral acts elicited by stimulation of single, identifiable brain cells. Science 157:570–574

    PubMed  CAS  Google Scholar 

  • Willows AOD, Dorsett DA, Hoyle G (1973) The neuronal basis of behavior in Tritonia. I. Functional organization of the central nervous system. J Neurobiol 4:207–237

    PubMed  CAS  Google Scholar 

  • Wilson JA, Phillips CE, Adams ME, Huber F (1982) Structural comparison of a homologous neuron in gryllid and acridid insects. J Neurobiol 13:459–467

    PubMed  CAS  Google Scholar 

  • Wollscheid-Lengeling E, Boore J, Brown W, Wägele H (2001) The phylogeny of Nudibranchia (Opisthobranchia, Gastropoda, Mollusca) reconstructed by three molecular markers. Org Divers Evol 1:241–256

    Google Scholar 

  • Wright WG (2000) Neuronal and behavioral plasticity in evolution: experiments in a model lineage. Bioscience 50:883–894

    Google Scholar 

  • Wright WG, Jones K, Sharp P, Maynard B (1995) Widespread anatomical projections of the serotonergic modulatory neuron, CB1, in Aplysia. Invert Neurosci 1:173–183

    PubMed  CAS  Google Scholar 

  • Xin Y, Koester J, Jing J, Weiss KR, Kupfermann I (2001) Cerebral–abdominal interganglionic coordinating neurons in Aplysia. J Neurophysiol 85:174–186

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Michael Baltzley for assistance in identifying Pd5 homologues, Evan Hill and Akira Sakurai for providing dye fills of Tritonia DSIs, Birgit Neuhaus and Priyal Shah for acquiring the confocal images, and Akira Sakurai for assistance with the spike shape analysis. We also thank Michael Baltzley, Shaun Cain, David Duggins, Erica Iyengar, James Murray, Thomas Pirtle, and Winsor Watson for collecting animals. Ronald Calabrese, Robert Calin-Jageman, Charles Derby, Joshua Lillvis, Dorothy Paul, Akira Sakurai, and two anonymous reviewers provided valuable comments on earlier versions of this manuscript. These experiments complied with the “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of the USA.

Author information

Author notes

  1. James M. Newcomb

    Present address: Department of Biology, NEC Box # 29, New England College, 24 Bridge St, Henniker, NH 03242-3296, USA

Authors and Affiliations

  1. Department of Biology, Georgia State University, P.O. Box 4010, Atlanta, GA, 30302-4010, USA

    James M. Newcomb & Paul S. Katz

Authors
  1. James M. Newcomb
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul S. Katz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul S. Katz.

Additional information

This material is based upon work supported by the National Science Foundation, under Grant No. 0445768, and a GSU Research Program Enhancement grant to PSK.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Newcomb, J.M., Katz, P.S. Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors. J Comp Physiol A 193, 425–443 (2007). https://doi.org/10.1007/s00359-006-0196-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-006-0196-4

Keywords

Search

Navigation