Identification and Characterization of Catecholaminergic Neuron B65, Which Initiates and Modifies Patterned Activity in the Buccal Ganglia of Aplysia

1998 ◽  
Vol 79 (2) ◽  
pp. 605-621 ◽  
Author(s):  
E. A. Kabotyanski ◽  
D. A. Baxter ◽  
J. H. Byrne
Keyword(s):  
Motor Neurons ◽  
Functional Organization ◽  
Synaptic Connections ◽  
Feeding Behaviors ◽  
Postsynaptic Potentials ◽  
Buccal Ganglia ◽  
Bath Application ◽  
Catecholaminergic Neuron ◽  
Identification And Characterization

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.

Connections between thoraco-coxal proprioceptive afferents and motor neurons in the locust

2000 ◽  
Vol 203 (3) ◽  
pp. 435-445
Author(s):  
M. Wildman
Keyword(s):  
Electrical Stimulation ◽  
Sensory Neurons ◽  
Motor Neurons ◽  
Chordotonal Organ ◽  
Synaptic Connections ◽  
Afferent Neurons ◽  
Postsynaptic Potentials ◽  
The Common ◽  
Proprioceptive Afferents ◽  
Stimulation Of

The position of the coxal segment of the locust hind leg relative to the thorax is monitored by a variety of proprioceptors, including three chordotonal organs and a myochordotonal organ. The sensory neurons of two of these proprioceptors, the posterior joint chordotonal organ (pjCO) and the myochordotonal organ (MCO), have axons in the purely sensory metathoracic nerve 2C (N2C). The connections made by these afferents with metathoracic motor neurons innervating thoraco-coxal and wing muscles were investigated by electrical stimulation of N2C and by matching postsynaptic potentials in motor neurons with afferent spikes in N2C. Stretch applied to the anterior rotator muscle of the coxa (M121), with which the MCO is associated, evoked sensory spikes in N2C. Some of the MCO afferent neurons make direct excitatory chemical synaptic connections with motor neurons innervating the thoraco-coxal muscles M121, M126 and M125. Parallel polysynaptic pathways via unidentified interneurons also exist between MCO afferents and these motor neurons. Connections with the common inhibitor 1 neuron and motor neurons innervating the thoraco-coxal muscles M123/4 and wing muscles M113 and M127 are polysynaptic. Afferents of the pjCO also make polysynaptic connections with motor neurons innervating thoraco-coxal and wing muscles, but no evidence for monosynaptic pathways was found.

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
Keyword(s):  
Feeding Activity ◽  
Neural Correlates ◽  
Neural Circuitry ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Rhythmic Movements ◽  
Motor Programs ◽  
Dopaminergic Cells ◽  
Buccal Ganglia ◽  
Bath Application

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.

Fast Synaptic Connections From CBIs to Pattern-Generating Neurons in Aplysia: Initiation and Modification of Motor Programs

2003 ◽  
Vol 89 (4) ◽  
pp. 2120-2136 ◽  
Author(s):  
Itay Hurwitz ◽  
Irving Kupfermann ◽  
Klaudiusz R. Weiss
Keyword(s):  
Central Pattern Generator ◽  
Motor Pattern ◽  
Aplysia Californica ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Motor Patterns ◽  
Motor Programs ◽  
Postsynaptic Potentials ◽  
Buccal Ganglia ◽  
Very High

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.

Conditional Rhythmicity and Synchrony in a Bilateral Pair of Bursting Motor Neurons in Aplysia

2006 ◽  
Vol 96 (4) ◽  
pp. 2056-2071 ◽  
Author(s):  
Geidy E. Serrano ◽  
Mark W. Miller
Keyword(s):  
Motor Neurons ◽  
Aplysia Californica ◽  
Burst Activity ◽  
Feeding System ◽  
Postsynaptic Potentials ◽  
Potential Source ◽  
Bath Application ◽  
Bilateral Pair ◽  
Driver Potential ◽  
Rhythmic Burst

This investigation examined the activity of a bilateral pair of motor neurons (B67) in the feeding system of Aplysia californica. In isolated ganglia, B67 firing exhibited a highly stereotyped bursting pattern that could be attributed to an underlying TTX-resistant driver potential (DP). Under control conditions, this bursting in the two B67 neurons was infrequent, irregular, and asynchronous. However, bath application of the neuromodulator dopamine (DA) increased the duration, frequency, rhythmicity, and synchrony of B67 bursts. In the absence of DA, depolarization of B67 with injected current produced rhythmic bursting. Such depolarization-induced rhythmic burst activity in one B67, however, did not entrain its contralateral counterpart. Moreover, when both B67s were depolarized to potentials that produced rhythmic bursting, their synchrony was significantly lower than that produced by DA. In TTX, dopamine increased the DP duration, enhanced the amplitude of slow signaling between the two B67s, and increased DP synchrony. A potential source of dopaminergic signaling to B67 was identified as B65, an influential interneuron with bilateral buccal projections. Firing B65 produced bursts in the ipsilateral and contralateral B67s. Under conditions that attenuated polysynaptic activity, firing B65 evoked rapid excitatory postsynaptic potentials in B67 that were blocked by sulpiride, an antagonist of synaptic DA receptors in this system. Finally, firing a single B65 was capable of producing a prolonged period of rhythmic synchronous bursting of the paired B67s. It is proposed that modulatory dopaminergic signaling originating from B65 during consummatory behaviors can promote rhythmicity and bilateral synchrony in the paired B67 motor neurons.

scholarly journals Phase-Locked Coordination Between Two Rhythmically Active Feeding Structures in the Mollusk Clione limacina. I. Motor Neurons

2002 ◽  
Vol 87 (6) ◽  
pp. 2996-3005 ◽  
Author(s):  
Aleksey Y. Malyshev ◽  
Tigran P. Norekian
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Electrical Coupling ◽  
Pattern Generator ◽  
Dependent Manner ◽  
Synaptic Connections ◽  
Buccal Ganglia ◽  
Active Feeding ◽  
Clione Limacina ◽  
Specific Phase

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.

Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: synaptic connections, effects on ongoing motor rhythms, and peptide modulation

1990 ◽  
Vol 63 (3) ◽  
pp. 539-558 ◽  
Author(s):  
M. R. Plummer ◽  
M. D. Kirk
Keyword(s):  
Cell Body ◽  
Motor Neurons ◽  
Firing Frequency ◽  
Inhibitory Synapses ◽  
Adjacent Cell ◽  
Synaptic Connections ◽  
Synaptic Potentials ◽  
Buccal Ganglia ◽  
Premotor Neurons ◽  
Electrical Connections

1. Two buccal ganglia interneurons, labeled here as B51 and B52, have been identified on the basis of morphological and physiological criteria. 2. These neurons have multipolar cell bodies. B51 extends a major neurite, which arborizes in the neuropil ipsilateral to the soma; extends into the buccal commissure, where it branches profusely; and projects an axon out the radular nerve (n1); other processes emanating from the soma arborize in the adjacent cell body layer. B52 arborizes ipsilateral to its cell body and sends a major process out of the ipsilateral hemiganglion into the sheath that attaches the buccal ganglia to the buccal mass proper. Here the B52 axon projects through a previously undescribed structure, which forms an arch over the buccal commissure that we designate the commissural arch. The extraganglionic B52 axon sends several branches into the connective tissue and then returns to the contralateral hemiganglion, where it again branches. 3. Each neuron exhibits a unique set of physiological properties. B51 frequently produces plateau potentials, which persist and are even enhanced in solutions where Ca2+ is replaced with Co2+. On the other hand, B52 shows a powerful posthyperpolarization rebound that contributes to its burst formation during spontaneous and nerve-elicited cyclic motor output. 4. B51 and B52 display distinctive rhythmic bursting on stimulation of the radular nerve or esophageal nerve. Their burst-firing tended to occur at certain phase relationships with respect to firing in other buccal premotor and motor neurons. 5. When firing frequency is measured as a function of intracellularly injected current, B51 shows a steplike increase in firing with increasing current, whereas B52 firing frequency is continuously graded. 6. B51 and B52 were found to make extensive synaptic connections within the buccal ganglia. B51 exhibited primarily excitatory electrical connections with known premotor and motor neurons, including an electrotonic synapse with its contralateral homologue. 7. In contrast, B52 made bilateral inhibitory synapses with nearly all of the premotor and motor neurons of the ventral motor cluster. Most of these connections appeared to be monosynaptic, producing synaptic potentials with short and fixed latencies that persisted when the ganglia were bathed in solutions containing elevated concentrations of Ca2+ and Mg2+. 8. Other synaptic potentials produced by B52 were more variable in size and latency; these included slow inhibition of the B4 and B5 neurons and excitation of an identifiable neuron that projected out the radular nerve.(ABSTRACT TRUNCATED AT 400 WORDS)

An identified glutamatergic interneuron patterns feeding motor activity via both excitation and inhibition

1995 ◽  
Vol 73 (3) ◽  
pp. 945-956 ◽  
Author(s):  
E. M. Quinlan ◽  
K. Gregory ◽  
A. D. Murphy
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Activity Patterns ◽  
Motor Pattern ◽  
Neuron Activity ◽  
Inhibitory Effects ◽  
Standard Pattern ◽  
Glutamate Receptor Antagonist ◽  
Postsynaptic Potentials ◽  
Buccal Ganglia

1. Previously we demonstrated that glutamate is an important neurotransmitter in the CNS of Helisoma. Exogenous glutamate applied to the buccal ganglia mimicked both the excitatory and inhibitory effects of subunit 2 (S2) of the tripartite central pattern generator (CPG) on S2 postsynaptic motor neurons. Here we identify buccal interneuron B2 as an S2 interneuron by utilizing a combination of electrophysiology, pharmacology, and intracellular staining. In addition, neurons that were electrophysiologically and morphologically characterized as neuron B2 demonstrated antiglutamate immunoreactivity, suggesting that neuron B2 is a source of endogenous glutamate in the buccal ganglia. 2. Depolarization of neuron B2 evoked excitatory postsynaptic potentials in motor neurons excited by S2. The excitatory effects of B2 depolarization and S2 activation were reversibly antagonized by the ionotropic glutamate receptor antagonist 6-cyano-7-nitro-quinoxaline-2,3-dione, similar to the antagonism shown previously for application of exogenous glutamate. Depolarization of neuron B2 also evoked inhibitory postsynaptic potentials in motor neurons inhibited by S2. When such motor neurons were maintained in isolated cell culture, application of exogenous glutamate produced a direct hyperpolarization of the membrane potential. 3. The activity of neuron B2 is necessary for the production of the standard pattern of buccal motor neuron activity, which underlies functional feeding movements. The subunits of the tripartite buccal CPG must be active in the temporal sequence S1-S2-S3 to produce the standard feeding pattern. Rhythmic inhibition from neuron B2 terminated activity in S1 postsynaptic motor neurons and entrained the frequency of activity in S3 postsynaptic motor neurons. Hyperpolarization of neuron B2 disrupted the production of the standard motor pattern by eliminating S2 postsynaptic potentials in identified buccal motor neurons, thereby prolonging S1 activity and disrupting S3 bursting. 4. These data support the hypothesis that S2 neuron B2 is glutamatergic and demonstrate that glutamatergic transmission, and especially inhibition, is fundamental to the production of behaviorally critical motor neuron activity patterns in Helisoma.

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