Modulation of Fictive Feeding by Dopamine and Serotonin inAplysia

2000 ◽  
Vol 83 (1) ◽  
pp. 374-392 ◽  
Author(s):  
Evgeni A. Kabotyanski ◽  
Douglas A. Baxter ◽  
Susan J. Cushman ◽  
John H. Byrne

The buccal ganglia of Aplysia contain a central pattern generator (CPG) that mediates rhythmic movements of the buccal apparatus during feeding. Activity in this CPG is believed to be regulated, in part, by extrinsic serotonergic inputs and by an intrinsic and extrinsic system of putative dopaminergic cells. The present study investigated the roles of dopamine (DA) and serotonin (5-HT) in regulating feeding movements of the buccal apparatus and properties of the underlying neural circuitry. Perfusing a semi-intact head preparation with DA (50 μM) or the metabolic precursor of catecholamines (l-3–4-dihydroxyphenylalanine, DOPA, 250 μM) induced feeding-like movements of the jaws and radula/odontophore. These DA-induced movements were similar to bites in intact animals. Perfusing with 5-HT (5 μM) also induced feeding-like movements, but the 5-HT-induced movements were similar to swallows. In preparations of isolated buccal ganglia, buccal motor programs (BMPs) that represented at least two different aspects of fictive feeding (i.e., ingestion and rejection) could be recorded. Bath application of DA (50 μM) increased the frequency of BMPs, in part, by increasing the number of ingestion-like BMPs. Bath application of 5-HT (5 μM) did not significantly increase the frequency of BMPs nor did it significantly increase the proportion of ingestion-like BMPs being expressed. Many of the cells and synaptic connections within the CPG appeared to be modulated by DA or 5-HT. For example, bath application of DA decreased the excitability of cells B4/5 and B34, which in turn may have contributed to the DA-induced increase in ingestion-like BMPs. In summary, bite-like movements were induced by DA in the semi-intact preparation, and neural correlates of these DA-induced effects were manifest as an increase in ingestion-like BMPs in the isolated ganglia. Swallow-like movements were induced by 5-HT in the semi-intact preparation. Neural correlates of these 5-HT-induced effects were not evident in isolated buccal ganglia, however.

2003 ◽  
Vol 89 (4) ◽  
pp. 2120-2136 ◽  
Author(s):  
Itay Hurwitz ◽  
Irving Kupfermann ◽  
Klaudiusz R. Weiss

Consummatory feeding movements in Aplysia californica are organized by a central pattern generator (CPG) in the buccal ganglia. Buccal motor programs similar to those organized by the CPG are also initiated and controlled by the cerebro-buccal interneurons (CBIs), interneurons projecting from the cerebral to the buccal ganglia. To examine the mechanisms by which CBIs affect buccal motor programs, we have explored systematically the synaptic connections from three of the CBIs (CBI-1, CBI-2, CBI-3) to key buccal ganglia CPG neurons (B31/B32, B34, and B63). The CBIs were found to produce monosynaptic excitatory postsynaptic potentials (EPSPs) with both fast and slow components. In this report, we have characterized only the fast component. CBI-2 monosynaptically excites neurons B31/B32, B34, and B63, all of which can initiate motor programs when they are sufficiently stimulated. However, the ability of CBI-2 to initiate a program stems primarily from the excitation of B63. In B31/B32, the size of the EPSPs was relatively small and the threshold for excitation was very high. In addition, preventing firing in either B34 or B63 showed that only a block in B63 firing prevented CBI-2 from initiating programs in response to a brief stimulus. The connections from CBI-2 to the buccal ganglia neurons showed a prominent facilitation. The facilitation contributed to the ability of CBI-2 to initiate a BMP and also led to a change in the form of the BMP. The cholinergic blocker hexamethonium blocked the fast EPSPs induced by CBI-2 in buccal ganglia neurons and also blocked the EPSPs between a number of key CPG neurons within the buccal ganglia. CBI-2 and B63 were able to initiate motor patterns in hexamethonium, although the form of a motor pattern was changed, indicating that non-hexamethonium-sensitive receptors contribute to the ability of these cells to initiate bursts. By contrast to CBI-2, CBI-1 excited B63 but inhibited B34. CBI-3 excited B34 and not B63. The data indicate that CBI-1, -2, and -3 are components of a system that initiates and selects between buccal motor programs. Their behavioral function is likely to depend on which combination of CBIs and CPG elements are activated.


2002 ◽  
Vol 87 (6) ◽  
pp. 2996-3005 ◽  
Author(s):  
Aleksey Y. Malyshev ◽  
Tigran P. Norekian

Coordination between different motor centers is essential for the orderly production of all complex behaviors, in both vertebrates and invertebrates. The current study revealed that rhythmic activities of two feeding structures of the pteropod mollusk Clione limacina, radula and hooks, which are used to extract the prey from its shell, are highly coordinated in a phase-dependent manner. Hook protraction always coincided with radula retraction, while hook retraction coincided with radula protraction. Thus hooks and radula were always moving in the opposite phases, taking turns grabbing and pulling the prey tissue out of the shell. Identified buccal ganglia motor neurons controlling radula and hooks protraction and retraction were rhythmically active in the same phase-dependent manner. Hook protractor motor neurons were active in the same phase with radula retractor motor neurons, while hook retractor motor neurons burst in phase with radula protractor motor neurons. One of the main mechanisms underlying the phase-locked coordination was electrical coupling between hook protractor and radula retractor motor neurons. In addition, reciprocal inhibitory synaptic connections were found between hook protractor and radula protractor motor neurons. These electrical and inhibitory synaptic connections ensure that rhythmically active hooks and radula controlling motor neurons are coordinated in the specific phase-dependent manner described above. The possible existence of a single multifunctional central pattern generator for both radula and hook motor centers is discussed.


2000 ◽  
Vol 84 (6) ◽  
pp. 2961-2974 ◽  
Author(s):  
José Antonio D. Sánchez ◽  
Yongsheng Li ◽  
Mark D. Kirk

In the sea slug Aplysia, rhythmic biting is eliminated after bilateral cerebral-buccal connective (CBC) crushes and recovers within 14 days postlesion (dpl). The ability of cerebral-buccal interneuron-2 (CBI-2) to elicit ingestion buccal motor programs (iBMPs; i.e., fictive rhythmic ingestion) and to regenerate synaptic connections with target buccal neurons was assessed with intracellular recordings and dye injections. Isolated central ganglia were obtained from control animals and from lesioned animals at selected times after bilateral CBC crushes. Within 3 wk postlesion, transected CBI-2 axons sprouted at least 10 fine neurites confined to the core of the CBC that projected across the crush site toward the buccal ganglia. When fired with depolarizing current steps, CBI-2 was not observed to elicit iBMPs in preparations until 14 dpl. Thereafter a progressive enhancement in CBI-2's ability to elicit iBMPs was observed with time postlesion. By 40 dpl, CBI-2-elicited iBMPs were indistinguishable from those of controls. CBI-2 regenerated monosynaptic connections with appropriate buccal premotor- and motorneurons by 14 dpl, and the strength of these connections increased with time postlesion. Dramatic frequency facilitation was exhibited by the regenerating CBI-2 buccal synapses; for instance, at early postlesion times, no observable excitatory postsynaptic potentials (EPSPs) were obtained with 1- Hz stimulation of CBI-2, while at 7 Hz, a dramatic increase in EPSP amplitude was obtained with successive spikes. The present study shows that the time course of axonal and synaptic regeneration by command-like interneuron CBI-2 is correlated with the recovery of ingestion buccal motor programs elicited by CBI-2. These results parallel our previous findings of functional neural regeneration in the feeding system and suggest that functional neural regeneration is at least in part mediated by regeneration of specific synaptic pathways.


1998 ◽  
Vol 79 (2) ◽  
pp. 605-621 ◽  
Author(s):  
E. A. Kabotyanski ◽  
D. A. Baxter ◽  
J. H. Byrne

Kabotyanski, E. A., D. A. Baxter, and J. H. Byrne. Identification and characterization of catecholaminergic neuron B65, which initiates and modifies patterned activity in the buccal ganglia of Aplysia. J. Neurophysiol. 79: 605–621, 1998. Catecholamines are believed to play an important role in regulating the properties and functional organization of the neural circuitry mediating consummatory feeding behaviors in Aplysia. In the present study, we morphologically and electrophysiologically identified a pair of catecholaminergic interneurons, referred to as B65, in the buccal ganglia. Their processes innervate both the ipsi- and contralateral neuropil, and separate branches of B65 appeared to innervate the somata of both ipsi- and contralateral B4/5 neurons. B65 exhibited patterned burst(s) of activity during spontaneous cycles of fictive feeding. Patterned activity in B65 also was elicited by stimulation of the radula nerve, by depolarization of the pattern initiating neurons B31/32 or B63, and by bath application of l-3,4-dihydroxyphenylalanine (DOPA). B65 appeared to be a member of the protraction group of neurons. Action potentials in B65 elicited fast one-for-one excitatory postsynaptic potentials (EPSPs) in neurons B4/5, B8A/B, B31/32, B63, and B64. In turn, B31/32 and B63 excited B65 and B64 inhibited B65. Some of the synaptic connections of B65 were plastic. For example, the fast EPSPs elicited in B4/5 and B64 decremented, whereas those in B31/32 andB8A/B facilitated. In addition to fast EPSPs, B65 elicited slow postsynaptic potentials in some of its follower cells. Depolarization of B65 elicited cycles of patterned activity indicative of fictive feeding in buccal neurons, including B65 itself. During series of B65-induced patterns, the properties of the buccal motor programs appeared to change. In particular, the activity of radula closure motor neurons B8A/B, which initially coincided mainly with the protraction phase of a cycle, gradually extended to overlap mostly with the retraction phase. This observation suggests that prolonged activity in B65 may play a role in transitioning from rejection-like to ingestion-like fictive feeding. The phase shift of the activity of B8A/B appears due, at least in part, to a decrease in activity of B4/5, and thus a reduction in inhibition from B4/5 onto B8A/B, during the retraction phase. The functional properties and synaptic connections of B65 suggest that it may play an important role in determining features of patterned neural activity in the buccal ganglia.


1994 ◽  
Vol 71 (1) ◽  
pp. 294-308 ◽  
Author(s):  
I. Ziv ◽  
D. A. Baxter ◽  
J. H. Byrne

1. We describe a simulator for neural networks and action potentials (SNNAP) that can simulate up to 30 neurons, each with up to 30 voltage-dependent conductances, 30 electrical synapses, and 30 multicomponent chemical synapses. Voltage-dependent conductances are described by Hodgkin-Huxley type equations, and the contributions of time-dependent synaptic conductances are described by second-order differential equations. The program also incorporates equations for simulating different types of neural modulation and synaptic plasticity. 2. Parameters, initial conditions, and output options for SNNAP are passed to the program through a number of modular ASCII files. These modules can be modified by commonly available text editors that use a conventional (i.e., character based) interface or by an editor incorporated into SNNAP that uses a graphical interface. The modular design facilitates the incorporation of existing modules into new simulations. Thus libraries can be developed of files describing distinctive cell types and files describing distinctive neural networks. 3. Several different types of neurons with distinct biophysical properties and firing properties were simulated by incorporating different combinations of voltage-dependent Na+, Ca2+, and K+ channels as well as Ca(2+)-activated and Ca(2+)-inactivated channels. Simulated cells included those that respond to depolarization with tonic firing, adaptive firing, or plateau potentials as well as endogenous pacemaker and bursting cells. 4. Several types of simple neural networks were simulated that included feed-forward excitatory and inhibitory chemical synaptic connections, a network of electrically coupled cells, and a network with feedback chemical synaptic connections that simulated rhythmic neural activity. In addition, with the use of the equations describing electrical coupling, current flow in a branched neuron with 18 compartments was simulated. 5. Enhancement of excitability and enhancement of transmitter release, produced by modulatory transmitters, were simulated by second-messenger-induced modulation of K+ currents. A depletion model for synaptic depression was also simulated. 6. We also attempted to simulate the features of a more complicated central pattern generator, inspired by the properties of neurons in the buccal ganglia of Aplysia. Dynamic changes in the activity of this central pattern generator were produced by a second-messenger-induced modulation of a slow inward current in one of the neurons.


1982 ◽  
Vol 99 (1) ◽  
pp. 197-205 ◽  
Author(s):  
J. A. Kahn ◽  
A. Roberts

Xenopus embryos struggle when restrained. Struggling involves rhythmic movements of large amplitude, in which waves of bending propagate from the tail to the head. Underlying this, electrical activity in myotomal muscles occurs in rhythmic bursts that alternate on either side of a segment. Bursts in ipsilateral segments occur in a caudo-rostral sequence. Curarized embryos can generate motor nerve activity in a struggling pattern in the absence of rhythmic sensory stimulation; the pattern is therefore produced by a central pattern generator.


1979 ◽  
Vol 79 (1) ◽  
pp. 23-40
Author(s):  
A.G. M. BULLOCH ◽  
D. A. DORSETT

Three phases of activity may be recognized in the buccal mass of Tritonia hombergi during the feeding cycle. These have been termed Protraction, Retraction and Flattening. Each phase is driven by a group of motoneurones along the posterior border of the buccal ganglia. The patterned bursting observed in the motoneurone groups during feeding activity is phased by synaptic inputs which are common to two or more groups. Evidence is presented which indicates these inputs are derived from three unidentified multi-action interneurone sources within each buccal ganglion, and whose action primarily determines the patterned output of the motoneurones. Electrical coupling between between synergistic motoneurones and, in one case, post-inhibitory rebound, contribute to the synchronization of group activity. Proprioceptive input to the motoneurones was not identified, but may project to the interneurones. Some small neurones having synaptic inputs on the motoneurones appropriate to two of the interneurones were found, but require confirmation in this role. The cerebral giant cells synapse on representatives of three motoneurone groups, and also activate the buccal interneurones driving the feeding cycle. The patterned activity of the motoneurones can occur in the absence of cerebral cell activity.


2020 ◽  
Vol 2 (1) ◽  
Author(s):  
W H Watson ◽  
A Nash ◽  
C Lee ◽  
M D Patz ◽  
J M Newcomb

Synopsis The neuropeptide small cardioactive peptide (SCP) plays an integrative role in exciting various motor programs involved in feeding and locomotion in a number of gastropod species. In this study, immunohistochemistry, using monoclonal antibodies against SCPB, was used to localize SCPB-like-immunoreactive neurons in the central nervous system, and map their connections to various tissues, in the nudibranch, Melibe leonina. Approximately 28–36 SCPB-like-immunoreactive neurons were identified in the M. leonina brain, as well as one large neuron in each of the buccal ganglia. The neuropil of the pedal ganglia contained the most SCPB-like-immunoreactive varicosities, although only a small portion of these were due to SCPB-like-immunoreactive neurons in the same ganglion. This suggests that much of the SCPB-like immunoreactivity in the neuropil of the pedal ganglia was from neurons in other ganglia that projected through the pedal–pedal connectives or the connectives from the cerebral and pleural ganglia. We also observed extensive SCPB innervation along the length of the esophagus. Therefore, we investigated the impact of SCPB on locomotion in intact animals, as well as peristaltic contractions of the isolated esophagus. Injection of intact animals with SCPB at night led to a significant increase in crawling and swimming, compared to control animals injected with saline. Furthermore, perfusion of isolated brains with SCPB initiated expression of the swim motor program. Application of SCPB to the isolated quiescent esophagus initiated rhythmic peristaltic contractions, and this occurred in preparations both with and without the buccal ganglia being attached. All these data, taken together, suggest that SCPB could be released at night to arouse animals and enhance the expression of both feeding and swimming motor programs in M. leonina.


2000 ◽  
Vol 84 (3) ◽  
pp. 1186-1193 ◽  
Author(s):  
Peter T. Morgan ◽  
Ray Perrins ◽  
Philip E. Lloyd ◽  
Klaudiusz R. Weiss

Intrinsic and extrinsic neuromodulation are both thought to be responsible for the flexibility of the neural circuits (central pattern generators) that control rhythmic behaviors. Because the two forms of modulation have been studied in different circuits, it has been difficult to compare them directly. We find that the central pattern generator for biting in Aplysia is modulated both extrinsically and intrinsically. Both forms of modulation increase the frequency of motor programs and shorten the duration of the protraction phase. Extrinsic modulation is mediated by the serotonergic metacerebral cell (MCC) neurons and is mimicked by application of serotonin. Intrinsic modulation is mediated by the cerebral peptide-2 (CP-2) containing CBI-2 interneurons and is mimicked by application of CP-2. Since the effects of CBI-2 and CP-2 occlude each other, the modulatory actions of CBI-2 may be mediated by CP-2 release. Although the effects of intrinsic and extrinsic modulation are similar, the neurons that mediate them are active predominantly at different times, suggesting a specialized role for each system. Metacerebral cell (MCC) activity predominates in the preparatory (appetitive) phase and thus precedes the activation of CBI-2 and biting motor programs. Once the CBI-2s are activated and the biting motor program is initiated, MCC activity declines precipitously. Hence extrinsic modulation prefacilitates biting, whereas intrinsic modulation occurs during biting. Since biting inhibits appetitive behavior, intrinsic modulation cannot be used to prefacilitate biting in the appetitive phase. Thus the sequential use of extrinsic and intrinsic modulation may provide a means for premodulation of biting without the concomitant disruption of appetitive behaviors.


2020 ◽  
Vol 123 (4) ◽  
pp. 1566-1577 ◽  
Author(s):  
Koeun Lim ◽  
Wei Wang ◽  
Daniel M. Merfeld

We report novel neural correlates of predecisional choice confidence in frontal scalp potential in humans. In conjunction with the centroparietal choice-action event-related potential component, this new frontal choice confidence component further elucidates the dynamics of the frontoparietal decision-making neural circuitry.


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