Removal of spike frequency adaptation via neuromodulation intrinsic to the Tritonia escape swim central pattern generator (original) (raw)
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The Journal of neuroscience : the official journal of the Society for Neuroscience, 1995
Heterosynaptic enhancement of transmitter release is potentially very important for neuronal computation, yet, to our knowledge, no prior study has shown that stimulation of one neuron directly enhances release from an interneuron. Here, we demonstrate that in the marine mollusk Tritonia diomedea, the serotonergic dorsal swim interneurons (DSIs) heterosynaptically increase the amount of transmitter released from another interneuron, C2. Stimulation of a single DSI at physiological firing frequencies increases the size of synaptic potentials evoked by C2. This increase in synaptic efficacy is correlated with an increase in homosynaptic paired-pulse facilitation by C2. Thus, it is likely to be due to an enhancement of transmitter release from C2, rather than a postsynaptic action on the followers of C2. This is further supported by the fact that DSI stimulation enhances the strengths of all chemical synapses made by C2 within the swim network, regardless of their sign. Furthermore, DS...
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2002
Several motor networks have now been found to be multifunctional, in which one group of neurons participates in the generation of multiple behavioral motor programs. Not surprisingly, the behaviors involved are frequently closely related, often using the same or similar muscle groups. Here we describe an interneuronal network in the marine mollusk Tritonia diomedea that is involved in producing two highly dissimilar behaviors, rhythmic, muscle-based escape swimming and nonrhythmic, cilia-mediated crawling. Several observations support this conclusion. First, the dorsal swim interneurons (DSIs) of the swim central pattern generator (CPG) directly excite Pedal neuron 21 (Pd21) and Pd5, the only identified cilia-activating efferent neurons in Tritonia. Second, stimulation of a single DSI elicits beating of the foot cilia in semi-intact preparations and crawling in intact animal treadmill preparations. Third, the DSIs fire at an elevated rate for nearly 1 hr after a swim motor program, ...
Evidence That the Swim Afferent Neurons ofTritonia diomedeaAre Glutamatergic
The Biological Bulletin, 2009
The escape swim response of the marine mollusc Tritonia diomedea is a well-established model system for studies of the neural basis of behavior. While the swim neural network is reasonably well understood, little is known about the transmitters used by its constituent neurons. In the present study, we provide immunocytochemical and electrophysiological evidence that the S-cells, the afferent neurons that detect aversive skin stimuli and in turn trigger Tritonia's escape swim response, use glutamate as their transmitter. First, immunolabeling revealed that S-cell somata contain elevated levels of glutamate compared to most other neurons in the Tritonia brain, consistent with findings from glutamatergic neurons in many species. Second, pressure-applied puffs of glutamate produced the same excitatory response in the target neurons of the S-cells as the naturally released S-cell transmitter itself. Third, the glutamate receptor antagonist CNQX completely blocked S-cell synaptic connections. These findings support glutamate as a transmitter used by the S-cells, and will facilitate studies using this model system to explore a variety of issues related to the neural basis of behavior.
Journal of neurophysiology, 2007
Parameter space analysis suggests multi-site plasticity contributes to motor pattern initiation in Tritonia. J This research examines the mechanisms that initiate rhythmic activity in the episodic central pattern generator (CPG) underlying escape swimming in the gastropod mollusk Tritonia diomedea. Activation of the network is triggered by extrinsic excitatory input but also accompanied by intrinsic neuromodulation and the recruitment of additional excitation into the circuit. To examine how these factors influence circuit activation, a detailed simulation of the unmodulated CPG network was constructed from an extensive set of physiological measurements. In this model, extrinsic input alone is insufficient to initiate rhythmic activity, confirming that additional processes are involved in circuit activation. However, incorporating known neuromodulatory and polysynaptic effects into the model still failed to enable rhythmic activity, suggesting that additional circuit features are also required. To delineate the additional activation requirements, a large-scale parameter-space analysis was conducted (ϳ2 ϫ 10 6 configurations). The results suggest that initiation of the swim motor pattern requires substantial reconfiguration at multiple sites within the network, especially to recruit ventral swim interneuron-B (VSI) activity and increase coupling between the dorsal swim interneurons (DSIs) and cerebral neuron 2 (C2) coupling. Within the parameter space examined, we observed a tendency for rhythmic activity to be spontaneous and self-sustaining. This suggests that initiation of episodic rhythmic activity may involve temporarily restructuring a nonrhythmic network into a persistent oscillator. In particular, the time course of neuromodulatory effects may control both activation and termination of rhythmic bursting.
Sensitization of the Tritonia escape swim
Neurobiology of learning and memory, 1998
When repeatedly elicited, the oscillatory escape swim of the marine mollusc Tritonia diomedea undergoes habituation of the number of cycles per swim. Previous work has shown that this habituation is accompanied by sensitization of another feature of the behavior: latency to swim onset. Here we focused on the behavioral features of sensitization itself. Test swims elicited 5 min after a strong sensitizing head stimulus differed in several ways from control swims: sensitized animals had shorter latencies for gill and rhinophore withdrawal, a shorter latency for swim onset, a lower threshold for swim initiation, and an increased number of cycles per swim. Sensitized animals did not, however, swim any faster (no change in cycle period). A separate experiment found that swim onset latency also sensitized when Tritonia came into contact with one of their natural predators, the seastar Pycnopodia helianthoides, demonstrating the ecological relevance of this form of nonassociative learning....
Altering cAMP levels within a central pattern generator modifies or disrupts rhythmic motor output
Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology, 2007
Cyclic AMP is a second messenger that has been implicated in the neuromodulation of rhythmically active motor patterns. Here, we tested whether manipulating cAMP affects swim motor pattern generation in the mollusc, Tritonia diomedea. Inhibiting adenylyl cyclase (AC) with 9-cyclopentyladenine (9-CPA) slowed or stopped the swim motor pattern. Inhibiting phosphodiesterase with 3-isobutyl-1-methylxanthine (IBMX) or applying dibutyryl-cAMP (dB-cAMP) disrupted the swim motor pattern, as did iontophoresing cAMP into the central pattern generator neuron C2. Additionally, during wash-in, IBMX sometimes temporarily produced extended or spontaneous swim motor patterns. Photolysis of caged cAMP in C2 after initiation of the swim motor pattern inhibited subsequent bursting. These results suggest that cAMP levels can dynamically modulate swim motor pattern generation, possibly shaping the output of the central pattern generator on a cycle-by-cycle basis.
Prepulse Inhibition of theTritoniaEscape Swim
The Journal of Neuroscience, 1998
Presenting a weak stimulus just before a strong, startle stimulus reduces the amplitude of the ensuing startle response in humans and other vertebrates. This phenomenon, termed "prepulse inhibition" (PPI), appears to function to reduce distraction while processing sensory input. To date, no detailed neural mechanism has been described for PPI. Here we demonstrate PPI in the marine mollusk Tritonia diomedea, which has a nervous system highly suitable for cellular analyses. We found that a 100 msec vibrotactile prepulse prevented the animal's escape swim response to a closely following 1 sec tail shock. This inhibition was highly transient, with a significant effect lasting just 2.5 sec. These findings indicate that the Tritonia escape swim response undergoes a form of PPI phenomeno-logically similar to that observed in vertebrates. Further tests showed that the vibrotactile stimulus had no inhibitory effect if applied after tail shock, while the animal was preparing to swim, but it acted to terminate swims once they were actively under way. As a first step toward a cellular analysis of PPI, we recorded from neurons of the swim circuit in a semi-intact preparation and found that the vibrotactile stimulus used in the behavioral experiments also prevented the tail shock-elicited swim motor program. These results represent the first explicit demonstration of PPI in an invertebrate and establish Tritonia as a model system for analyzing its physiological basis.
The Journal of Physiology, 1998
If we are to understand motor coordination , it is important to define the synaptic input to motoneurones during normal motor behaviour and to ask whether this input remains the same in different parts of a rhythmic motor system which have different levels of rhythm-generating capacity. In many vertebrates glutamate is thought to provide most of the normal synaptic excitation during rhythmic motor activity. The first evidence for this is that such activity can be induced by the application of glutamate agonists. Activation of NMDA receptors evokes locomotor-like activity in the lamprey (
Parametric Features of Habituation of Swim Cycle Number in the Marine MolluscTritonia diomedea
Neurobiology of Learning and Memory, 1996
When repeatedly elicited, the oscillatory escape swim of the marine mollusc Tritonia diomedea undergoes habituation of the number of cycles per swim. Because the neural circuit for this behavior is reasonably well understood, a cellular analyses of habituation in Tritonia is feasible. Since such a study must ultimately relate cellular correlates to behavioral modifications, we have sought to increase our understanding of the parametric features of cycle number habituation in Tritonia. Habituation was compared when using different intertrial intervals, repeated training sessions, and different stimulus locations. Stimulus site generalization of habituation was demonstrated, suggesting that at least one site of plasticity underlying habitation is located postsynaptic to the sensory neurons for the response. Dishabituation from an above-zero baseline response level was not obtained. An isolated brain preparation was tested as a potential simplified system for cellular studies of habituation mechanisms. Repeated stimulation of a nerve containing sensory afferent processes resulted in a progressive reduction of swim motor program cycle number, with a rate similar to that seen in the behavior. Together, these findings: (1) establish a set of parametric features of cycle numbers habituation to be explained by physiological studies; (2) suggest that at least one circuit modification underlying the habituation is located among the circuit interneurons; and (3) indicate that the isolated brain preparation may serve as a useful neural analogue for studies of the cellular mechanisms of cycle number habituation in Tritonia.
Mechanism of frequency-dependent broadening of molluscan neurone soma spikes
The Journal of physiology, 1979
1. Action potentials recorded from isolated dorid neurone somata increase in duration, i.e. broaden, during low frequency repetitive firing. Spike broadening is substantially reduced by external Co ions and implicates an inward Ca current. 2. During repetitive voltage clamp steps at frequencies slower than 1 Hz, in 100 mM-tetraethyl ammonium ions (TEA) inward Ca currents do not increase in amplitude. 3. Repetitive action potentials result in inactivation of delayed outward current. Likewise, repetitive voltage clamp steps which cause inactivation of delayed outward current also result in longer duration action potentials. 4. The frequency dependence of spike broadening and inactivation of the voltage dependent component (IK) of delayed outward current are similar. 5. Inactivation of IK is observed in all cells, however, only cells with relative large inward Ca currents show significant spike broadening. Spike broadening apparently results from the frequency dependent inactivation of...