Swim Initiation Neurons in Tritonia diomedea1

Frost, William N.; Hoppe, Travis; Wang, J.; Tian, Lian-Ming

doi:10.1668/0003-1569(2001)041[0952:sinitd]2.0.co;2

Cited by 24 publications

(27 citation statements)

References 37 publications

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“…In the Tritonia swim system, neuron Tr1 fulfils the role of a trigger neuron ( Frost et al 2001), whereas DSI serves the role of a gating neuron within the swim CPG because hyperpolarizing this neuron will halt the swim motor pattern (Getting & Dekin 1985) and tonic spiking in these neurons is sufficient to maintain rhythmic activity ( Fickbohm & Katz 2000;Katz et al 2004). However, the dorsal ramp interneuron, which provides excitatory drive to DSI, better qualifies as a gating neuron because it is external to the CPG ( Frost & Katz 1996).…”

Section: Discussionmentioning

confidence: 99%

“…( f ) The Melibe CeSP-A neurons are homologous to the Tritonia DSIs. In Melibe, the CeSP-A neurons (black circles) resembled the Tritonia DSIs in several identifying characteristics, including number, soma location and axon projection pattern swim motor pattern , whereas activation of the DSIs can initiate a swim motor pattern ( Fickbohm & Katz 2000;Frost et al 2001;Katz et al 2004). Similarly, the DSI neurotransmitter, serotonin (5-HT), is also necessary and sufficient for initiating a swim motor pattern; application of 5-HT can initiate swimming in the animal and the swim motor pattern in the isolated nervous system, whereas the 5-HT antagonist, methysergide, can prevent the animal from swimming and prevent the production of the swim motor pattern in the isolated nervous system (McClellan et al 1994).…”

Section: Introductionmentioning

confidence: 99%

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Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

Newcomb

Katz

2008

Proc. R. Soc. B.

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Closely related species can exhibit different behaviours despite homologous neural substrates. The nudibranch molluscs Tritonia diomedea and Melibe leonina swim differently, yet their nervous systems contain homologous serotonergic neurons. In Tritonia, the dorsal swim interneurons (DSIs) are members of the swim central pattern generator (CPG) and their neurotransmitter serotonin is both necessary and sufficient to elicit a swim motor pattern. Here it is shown that the DSI homologues in Melibe, the cerebral serotonergic posterior-A neurons (CeSP-As), are extrinsic to the swim CPG, and that neither the CeSP-As nor their neurotransmitter serotonin is necessary for swim motor pattern initiation, which occurred when the CeSP-As were inactive. Furthermore, the serotonin antagonist methysergide blocked the effects of both the serotonin and CeSP-As but did not prevent the production of a swim motor pattern. However, the CeSP-As and serotonin could influence the Melibe swim circuit; depolarization of a cerebral serotonergic posterior-A was sufficient to initiate a swim motor pattern and hyperpolarization of a CeSP-A temporarily halted an ongoing swim motor pattern. Serotonin itself was sufficient to initiate a swim motor pattern or make an ongoing swim motor pattern more regular. Thus, evolution of species-specific behaviour involved alterations in the functions of identified homologous neurons and their neurotransmitter.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

Newcomb

Katz

2008

Proc. R. Soc. B.

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“…Blocking G protein signaling in a single C2 interrupts rhythmic motor pattern generation. Schematic representation of the CPG (black lines) and its input and output pathways (gray lines) (adapted from Frost et al 2001). Sensory neurons (S) transmit information both directly to the single dorsal ramp interneuron (DRI) and indirectly via a trigger neuron (Tr1).…”

Section: Injection Of Gdp-␤-s Into a Single C2 Blocked Motor Pattern mentioning

confidence: 99%

G Protein Signaling in a Neuronal Network is Necessary for Rhythmic Motor Pattern Production

Clemens

Katz

2003

Journal of Neurophysiology

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Clemens, Stefan, and Paul S. Katz. G protein signaling in a neuronal network is necessary for rhythmic motor pattern production. J Neurophysiol 89: 762-772, 2003; 10.1152/jn.00765.2002. G protein-coupled receptors are widely recognized as playing important roles in mediating the actions of extrinsic neuromodulatory inputs to motor networks. However, the potential for their direct involvement in rhythmic motor pattern generation has received considerably less attention. Results from this study indicate that G protein signaling appears to be integral to the operation of the central pattern generator (CPG) underlying the escape swim of the mollusk Tritonia diomedea. Blocking G protein signaling in a single CPG neuron, cerebral neuron C2, with intracellular iontophoresis of the guanine nucleotide analogue guanosine 5Ј-O-(2-thiodiphosphate) (GDP-␤-S), prevented the production of the swim motor program. Moreover, tonic activation of G protein signaling in this neuron by iontophoresis of the GTP analogues guanosine 5Ј-O-(3-thiotriphosphate) (GTP-␥-S) and 5Ј-guanylyl-imidodiphosphate also inhibited motor pattern production. The possible sites of action of these guanine nucleotide analogues were examined to assess potential mechanisms by which they interfered with motor pattern production. Intracellular iontophoresis of GDP-␤-S into C2 did not affect C2 basal synaptic strength. However, it did reduce heterosynaptic facilitation of C2 synapses caused by the dorsal swim interneurons (DSIs), a set of serotonergic swim CPG neurons. In contrast, GTP-␥-S directly enhanced C2 synaptic strength onto DFN, mimicking the neuromodulatory effect of the DSIs. GDP-␤-S, but not the GTP analogues, decreased C2 excitability, whereas both GTP analogues, but not GDP-␤-S, blocked the ability of DSI stimulation to increase C2 excitability. The decrease in C2 excitability caused by GDP-␤-S is not likely to be responsible for the inhibition of the swim motor pattern because decreasing C2 firing rate, by injecting hyperpolarizing current, did not prevent the production of the rhythmic motor pattern. Taken together, these data suggest that G protein signaling is a necessary and integral component of the escape swim CPG in Tritonia and that G protein signaling mediates DSI heterosynaptic facilitation of C2 but may not mediate the DSI-evoked enhancement of C2 excitability.

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“…Data acquisition and analysis were performed with Spike2 software (CED) and SigmaPlot (SPSS Inc.). Statistical comparisons were made using Student's t test, paired t test, or a one-way or two-way repeated-measures ANOVA with post hoc pairwise multiple comparison by Fisher's least Getting et al (1980), Getting (1981), Hume and Getting (1982), Frost and Katz (1996), and Frost et al (2001)]. B, Schematic drawing of a dorsal view of the Tritonia brain, showing the location of the swim CPG neurons and their axonal projections.…”

Section: Introductionmentioning

confidence: 99%

Functional Recovery after Lesion of a Central Pattern Generator

Sakurai¹,

Katz²

2009

J. Neurosci.

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In cases of neuronal injury when regeneration is restricted, functional recovery can occur through reorganization of the remaining neural circuitry. We found an example of such recovery in the central pattern generator (CPG) for the escape swim of the mollusc Tritonia diomedea. The CPG neurons are bilaterally represented and each neuron projects an axon through one of two pedal commissures. Cutting the posterior pedal commissure [pedal nerve 6 (PdN6)] in the animal or in the isolated brain caused a deficit in the swim behavior and in the fictive motor pattern, respectively, each of which recovered over the course of 20 h. Locally blocking spiking activity in PdN6 with sodium-free saline and/or tetrodotoxin disrupted the motor pattern in a reversible manner. Maintained blockade of PdN6 led to a functional recovery of the swim motor pattern similar to that observed in response to cutting the commissure. Among the CPG neurons, cerebral neuron 2 (C2) makes functional connection onto the ventral swim interneuron-B (VSI) in both pedal ganglia. Cutting or blocking PdN6 eliminated C2-evoked excitation of VSI in the pedal ganglion distal to the lesion. Associated with the recovery of the swim motor pattern, the synaptic action of C2 onto VSI in the proximal pedal ganglion changed from being predominantly inhibitory to being predominantly excitatory. These results show that the Tritonia swim CPG undergoes adaptive plasticity in response to the loss of critical synaptic connections; reversal of synaptic action in the CPG may be at least partially responsible for this functional recovery.

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Swim Initiation Neurons in Tritonia diomedea1

Cited by 24 publications

References 37 publications

Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

G Protein Signaling in a Neuronal Network is Necessary for Rhythmic Motor Pattern Production

Functional Recovery after Lesion of a Central Pattern Generator

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