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Tritonia

From Scholarpedia - Reading time: 7 min
Figure 1: Photo of Tritonia diomedea. Anterior is to the right. bt = Branchial Tufts, rh = Rhinophore, ov = Oral Veil.
Tritonia diomedea (Bergh, 1894)[1] is a nudibranch mollusc that has served as a model system for understanding the neural basis of behavior, cellular properties of neurons, and neuromodulation. It is particularly attractive because of the large size of its individual neurons (up to 800 microns), and its large variety of interesting behaviors, eg, escape swimming, magnetic field orientation, rheotaxis, crawling, feeding, mating. Work in the 1960s by A.O. Dennis Willows[2] was among the first to show the functions of single identified neurons in the production of behavior in any organism.


Contents

[edit] Species information

Figure 2: Two Tritonia mating.

Of the several "Tritonia" species most of the neurobiological research has been done on Tritonia diomedea. This animal lives in the Pacific Ocean coastal waters from Alaska to California. It feeds on soft coral such as sea pens, sea pansies, and sea whips. Not much is known about the ecology of the animal, but video studies in its natural habitat have contributed to our understanding of natural behavior (Wyeth and Willows, 2006a; Wyeth et al., 2006). As is true of other opisthobranchs, Tritonia is an obligate hermaphrodite, it can act as either male or female and must mate with another individual to reproduce. The sexual organs are located on the right side of the animal, so that animals pull up "starboard to starboard" to mate. They produce egg strands that can be raised in the lab. The eggs hatch to a planktotrophic veliger larva stage.

(Taxonomy ID: 70853 in NCBI Taxonomy browser)

Additional species of interest in the genus Tritonia include:

  1. Tritonia festiva
  2. Tritonia hombergi

[edit] Organization of the nervous system

Figure 3: Schematic of "Tritonia" central ganglia with some neuronal cell bodies marked. Ce=Cerebral Ganglion; Pl=Pleural Ganglion; Pd=Pedal Ganglion Body wall nerves are named after their ganglion of origin plus the number indicated. The identified neurons shown have contralateral counterparts. C1 is a giant serotonergic neuron that projects to the buccal ganglion. C2 is a peptidergic neuron involved in swimming. The cells marked 5,6 are Pedal 5 and 6, which are efferent peptidergic neurons. DSI are the Dorsal Swim Interneurons, a group of three serotonergic neurons in the swim CPG. The statocyst on the right is label, st.

The central nervous system is composed of the circumesophageal ring ganglia: cerebropleural, pedal (Pd), and buccal. The cerebropleural ganglion appears to represent a fusion between the cerebral (Ce) and pleural (Pl) in other opisthobranchs. Although these ganglia are fused, the neurons are often referred to as being in one or the other of the two ganglia.

The central ganglia consist of about 8000 individual neurons (Boyle et al., 1983). Some of these form clusters, others are uniquely identifiable. There are about 180 different types of neuron that have been identified in Tritonia. Notable neurons are shown in Figure 2. A complete list of neurons is cataloged in the "Tritonia" Branch of NeuronBank

[edit] Sensory Systems

Tritonia exhibits mechanosensivity and chemosensitivity over the surface of its body. There are sensory neurons with central cell bodies, called S-cells, which are bimodal, mechanoreceptors and chemoreceptors. As with other opisthobranchs, Tritonia has rhinophores that have a chemosensitive function (Wyeth and Willows 2006b).

Tritonia appears to be sensitive to water flow (Field and MacMillan 1973, Willows 1978). It tends to orient its body into the flow of water. The lateral branch of Cerebral Nerve 2 (CeN2) innervates the oral veil and carries information that is necessary (Murray and Willows 1996) for orientation to water flow, so-called rheotaxis.

One of the most striking sensory abilities of Tritonia, is its magnetoreception. Tritonia is capable of sensing Earth-strength magnetic fields and orienting to them. Correspondingly, efferent pedal neurons have been shown to change their firing in response to artificially altering the magnetic field. The mechanism for transduction of this sensory modality has not yet been determined.

Tritonia has no image forming eyes. As with other nudibranchs, it has photosensitive cells that are clustered together in the head region. Not much is known about the eyes (see however, Chase 1974). "Tritonia" also has statocysts that lie adjacent to the connective between the pleural and cerebral ganglia. These have not been examined in "Tritonia". See however, the related nudibranch Hermissenda.

[edit] Motor Systems

Motor responses that have been studied in this system include, feeding, gill withdrawal, ciliary locomotion, and swimming. The primary means of locomotion for Tritonia is mucociliary gliding in which the animal secretes mucus upon which it glides due to the action of cilia in the foot. Muscular movements do not seem to play a role in crawling, but may aid in turning (Redondo and Murray 2005). The rate of ciliary beating is controlled by efferent neurons in the pedal ganglia that contain serotonin and/or neuropeptides. In particular, a neuropeptide named Tritonia Pedal Peptide (Tpep) was shown to be released from giant pedal neurons and accelerate ciliary beating. A group of large neurons in the pedal ganglia, in particular, Pd5 and Pd6 are immunoreactive to Tpep.

Figure 4: Tritonia escape swimming. The picture shows a Tritonia escaping from a sea star, Pycnopodia. At the top are simultaneous intracellular electrophysiological recordings from the 3 central pattern generator (CPG) neurons: C2, DSI, and VSI taken from an isolated brain. At the arrow, a body wall nerve was stimulated, producing a pattern of discharges that lasts about a minute. DSI bursts alternate with VSI bursts producing dorsal and ventral body flexions. To the right is the neural circuit from sensory neurons to efferent output.
The other means of locomotion used by Tritonia is escape swimming in which the animal flattens its body (particularly its oral veil and tail) in the horizontal plane, and executes a series of 2-20 alternating dorsal-ventral body flexions. This serves to lift the animal off of the substrate so that water currents can carry it away to safety. The escape swim is performed in response to contact with the predatory sea star, Pycnopodia helianthoides. Tritonia will also swim in response to some other echinoderms, salt crystals or concentrated NaCl, or the bites of conspecifics. The CPG underlying this rhythmic behavior has been well studied. (See: Tritonia swim network). This CPG was one of the first to be reconstructed in realistic computer simulations. The CPG contains just three neuron types: Cerebral Interneuron 2 (C2), Dorsal Swim Interneuron (DSI-A,B,C, and Ventral Swim Interneuron (VSI-B).

The mechanism underlying production of the swim motor pattern is as follows. Sensory activation of the swim motor pattern is mediated by the S-cells. These neurons convey excitation to the Dorsal Ramp Interneuron (DRI) through Tr1, a trigger neuron. DRI, then excites the serotonergic DSIs. The DSIs excite C2 and also modulate its properties, allowing it to further recruit DRI firing. This sets up a positive feedback loop. VSI-B inhibits DSI and C2, momentarily interrupting the cycle. The CPG neurons excite efferent flexion neurons in the pedal ganglion (the dorsal flexion neurons (DFN) and the ventral flexion neurons (VFN)) that relay the activity to the muscles.

[edit] Behavioral Plasticity

The Tritonia swim response exhibits a number of forms of behavioral plasticity. When repeatedly stimulated to swim, the animal and the isolated nervous system exhibit habituation, evident by a progressive reduction in flexion cycles per swim. The animal and the isolated nervous system also exhibit sensitization, evident by a period of enhanced swim responsiveness. The Tritonia swim response also exhibits prepulse inhibition, where prior tactile stimulation will briefly suppress the ability of other stimuli to elicit the swim.

[edit] Cellular and Synaptic Actions

The DSIs of the swim CPG are serotonergic and have neuromodulatory actions on other members of the swim CPG. This was termed Intrinsic Neuromodulation because the neuromodulation was coming from within the circuit as opposed to from elements outside the circuit. The modulatory actions of the DSIs can be complex, producing what has been called Spike-timing-dependent neuromodulation.

[edit] References

  1. Audesirk G (1978) Central neuronal control of cilia in Tritonia diomedia [sic]. Nature 272:541-543.
  2. Beck JC, Cooper MS, Willows AOD (2000) Immunocytochemical localization of pedal peptide in the central nervous system of the gastropod mollusc Tritonia diomedea. J Comp Neurol 425:1-9.
  3. Boyle MB, Cohen LB, Macagno ER, Orbach H (1983) The number and size of neurons in the CNS of gastropod molluscs and their suitability for optical recording of activity. Brain Res 266:305-317
  4. Chase R (1974) The electrophysiology of photoreceptors in the nudibranch mollusc, Tritonia diomedia. J Exp Biol 60:707-719.
  5. Dorsett DA, Willows AOD (1974) Interactions between neurons mediating tuft withdrawal in Tritonia hombergi. J Exp Biol 61:655-666.
  6. Dorsett DA, Willows AOD, Hoyle G (1969) Centrally generated nerve impulse sequences determining swimming behavior in Tritonia. Nature 224:711-712.
  7. Field LH, MacMillan DL (1973) An electrophysiological and behavioral study of sensory responses in Tritonia (Gastropoda, Nudibranchia). Mar Behav Physiol 2:171-185
  8. Frost WN, Tian LM, Hoppe TA, Mongeluzi DL, Wang J (2003) A cellular mechanism for prepulse inhibition. Neuron 40:991-1001.
  9. Getting PA (1981) Mechanisms of pattern generation underlying swimming in Tritonia. I. Neuronal network formed by monosynaptic connections. J Neurophysiol 46:65-79.
  10. Getting PA (1989) A network oscillator underlying swimming in Tritonia. In: Neuronal and Cellular Oscillators (Jacklet JW, ed), pp 215-236. New York: Marcel Dekker, Inc.
  11. Getting PA, Dekin MS (1985) Tritonia swimming: a model system for integration within rhythmic motor systems. In: Model Neural Networks and Behavior (Selverston AI, ed), pp 3-20. New York: Plenum Press.
  12. Getting PA, Lennard PR, Hume RI (1980) Central pattern generator mediating swimming in Tritonia. I. Identification and synaptic interactions. J Neurophysiol 44:151-164.
  13. Katz PS, Frost WN (1995) Intrinsic neuromodulation in the Tritonia swim CPG: The serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2. J Neurosci 15:6035-6045.
  14. Katz PS, Getting PA, Frost WN (1994) Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367:729-731.
  15. Lloyd PE, Phares GA, Phillips NE, Willows AOD (1996) Purification and sequencing of neuropeptides from identified neurons in the marine mollusc, Tritonia. Peptides 17:17-23.
  16. Lohmann KJ, Willows AO (1987) Lunar-modulated geomagnetic orientation by a marine mollusk. Science 235:331-334.
  17. Lohmann KJ, Willows AO, Pinter RB (1991) An identifiable molluscan neuron responds to changes in earth- strength magnetic fields. J Exp Biol 161:1-24.
  18. McCaman MW, Weinreich D, McCaman RE (1973) The determination of picomole levels of 5-hydroxytryptamine and dopamine in Aplysia, Tritonia and leech nervous tissues. Brain Res 53:129-137.
  19. Mongeluzi DL, Frost WN (2000) Dishabituation of the Tritonia escape swim. Learn Mem 7:43-47.
  20. Mongeluzi DL, Hoppe TA, Frost WN (1998) Prepulse Inhibition of the Tritonia Escape Swim. J Neurosci 18:8467-8472.
  21. Murray JA, Hewes RS, Willows AOD (1992) Water-flow sensitive pedal neurons in Tritonia: Role in rheotaxis. J Comp Physiol A 171:373-385.
  22. Murray JA, Willows AOD (1996) Function of identified nerves in orientation to water flow in Tritonia diomedea. J Comp Physiol A 178:201-209.
  23. Redondo RL , Murray JA (2005) A single neuron serves a significant role in effecting turning while crawling in the marine slug Tritonia diomedea (Bergh), Journal of Comparative Physiology A 191:435-444 [PubMed 15778839]
  24. 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.
  25. Thompson SH (1977) Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol (Lond) 265:465-488.
  26. Willows AO (1967) Behavioral acts elicited by stimulation of single, identifiable brain cells. Science 157:570-574. PMID: 4700705 [3]
  27. 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.
  28. Willows AOD, Hoyle G (1969) Neuronal network triggering of fixed action pattern. Science 166:1549-1551.
  29. Willows AOD, Lloyd PE, Masinovsky BP (1988) Multiple transmitter neurons in Tritonia. III. Modulation of central pattern generator controlling feeding. J Neurobiol 19:69-86.
  30. Wyeth RC, Willows AO (2006a) Field behavior of the nudibranch mollusc Tritonia diomedea. Biol Bull 210:81-96.
  31. Wyeth RC, Willows AO (2006b) Odours detected by rhinophores mediate orientation to flow in the nudibranch mollusc, Tritonia diomedea. J Exp Biol 209:1441-1453.
  32. Wyeth RC, Woodward OM, Willows AOD. 2006c. Orientation and navigation relative to water flow, prey, conspecifics and predators by the nudibranch mollusc, Tritonia diomedea. Biol Bull 210:97-108


[edit] Links to additional information


[edit] See Also

Tritonia Swim Network,,,

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