Glutamate as a putative neurotransmitter in the buccal central pattern generator of Helisoma trivolvis

1991 ◽  
Vol 66 (4) ◽  
pp. 1264-1271 ◽  
Author(s):  
E. M. Quinlan ◽  
A. D. Murphy

1. The effects of L-glutamate superfusion over identified neurons within the buccal ganglia of Helisoma trivolvis were examined. Glutamate mirrored the effect of activity of subunit 2 (S2) of the tripartite feeding central pattern generator (CPG) on S2 postsynaptic neurons. Neurons that are excited by S2 are depolarized by glutamate, whereas neurons that are inhibited by S2 are hyperpolarized by glutamate. Glutamate also stimulated rhythmic S2 activity. 2. Different glutamate agonists could mimic specific components of the effects of glutamate on buccal neurons. Kainate produced depolarizations in neurons that receive S2 excitatory postsynaptic potentials (EPSPs) and activated rhythmic S2 activity. Quisqualate produced hyperpolarizations in neurons that receive S2 inhibitory postsynaptic potentials (IPSPs). 3. The non-N-methyl-D-aspartate glutamate receptor antagonist cyano-7-nitroquinoxaline-2,3-dione (CNQX) blocked the effects of S2 EPSPs and depolarizations produced by application of glutamate and kainate, but was ineffective in blocking S2 IPSPs or hyperpolarizations produced by application of glutamate and quisqualate. 4. These data support the hypothesis that glutamate is the transmitter of S2 of the feeding CPG in Helisoma, acting at CNQX-sensitive kainate-like receptors at excitatory synapses and CNQX-insensitive quisqualate-like receptors at inhibitory synapses.

1989 ◽  
Vol 147 (1) ◽  
pp. 361-374
Author(s):  
CATHERINE R. McCROHAN ◽  
MICHAEL A. KYRIAKIDES

1. The cerebral ventral 1 (CV1) interneurones of Lymnaea occurred as a population of at least three in each ganglion, all with similar morphologies. Steady depolarization of a CV1 cell led to initiation and maintenance of rhythmic feeding motor output from the buccal ganglia. 2. CV1 interneurones produced facilitating excitatory postsynaptic potentials in Nl interneurones of the buccal central pattern generator for feeding. Connections with N2 interneurones were not found. 3. The CV1 population could be separated into two subgroups. CVla received strong synaptic feedback in phase with the buccal rhythm, leading to strong bursting during generation of feeding motor output. CVlb received only weak feedback, and often fired continuously when depolarized. 4. Unitary inhibitory postsynaptic potentials were characteristic of all CV1 neurones, but were only visible in CVlb when it was depolarized. These inputs are thought to arise indirectly from the buccal central pattern generator. 5. The CV1 population is probably homologous with similar neurones in other gastropod species.


1988 ◽  
Vol 59 (1) ◽  
pp. 110-123 ◽  
Author(s):  
E. P. Christian ◽  
F. E. Dudek

1. Evidence for local excitatory synaptic connections in CA1 of the rat hippocampus was obtained by recording excitatory postsynaptic potentials (EPSPs) intracellularly from pyramidal cells during local microapplications of glutamate. 2. Experiments were performed in hippocampal slices cut parallel to (transverse slice) or perpendicular to (longitudinal slice) alvear fibers. In normal solutions, glutamate microdrops (10–20 mM, 10–20 micron diam) applied in CA1 within 400 micron of recorded cells sometimes increased the frequency of inhibitory postsynaptic potentials for 5–10 s in both transverse and longitudinal slices. Increases in EPSP frequency were also occasionally observed, but only in transverse slices. Tetrodotoxin (1 microgram/ml) blocked glutamate-induced increases in PSP frequency, thus indicating that they were not caused by subthreshold effects on presynaptic terminals. Increases in PSP frequency were interpreted to result from glutamate activation of hippocampal neurons with inhibitory and excitatory connections to recorded neurons. 3. In both slice orientations, local excitatory circuits were studied in more isolated conditions by surgically separating CA1 from CA3 (transverse slices) and by blocking GABAergic inhibitory synapses with picrotoxin (5–10 microM). Microdrops were systematically applied at 200 and 400 micron on each side of the recording site. Significant glutamate-induced increases in EPSP frequency were observed in neurons from both slice orientations to microdrops in at least one of the locations. This provided evidence that excitatory synapses are present in both transverse and longitudinal slices. 4. Substantial increases in EPSP frequency only occurred in neurons from longitudinal slices when glutamate was microapplied 200 micron or less from the recording site. In transverse slices, however, large increases in EPSP frequency were observed to glutamate microapplications at 200 or 400 micron. These data suggest that CA1 local excitatory connections project for longer distances in the transverse than in the longitudinal plane of section. 5. Increases in EPSP frequency, averaged across cells, did not differ significantly in the four microapplication sites in either transverse or longitudinal slices. Thus local excitation in CA1 does not appear to be asymmetrically arranged in the way suggested for CA3. 6. The densities of local excitatory circuits in CA1 versus CA3 were studied by quantitatively comparing glutamate-induced increases in EPSP frequency.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


1995 ◽  
Vol 73 (1) ◽  
pp. 112-124 ◽  
Author(s):  
M. S. Yeoman ◽  
A. Vehovszky ◽  
G. Kemenes ◽  
C. J. Elliott ◽  
P. R. Benjamin

1. We used intracellular recording techniques to examine the role of a novel type of protraction phase interneuron, the lateral N1 (N1L) in the feeding system of the snail Lymnaea stagnalis. 2. The N1Ls are a bilaterally symmetrical pair of electrotonically coupled interneurons located in the buccal ganglia. Each N1L sends a single axon to the contralateral buccal ganglia. Their neurite processes are confined to the buccal neuropile. 3. In the isolated CNS, depolarization of an N1L is capable of driving a full (N1-->N2-->N3), fast (1 cycle every 5 s) fictive feeding rhythm. This was unlike the previously described N1 medial (N1M) central pattern generator (CPG) interneurons that were only capable of driving a slow, irregular rhythm. Attempts to control the frequency of the fictive feeding rhythm by injecting varying amounts of steady current into the N1Ls were unsuccessful. This contrasts with a modulatory neuron, the slow oscillator (SO), that has very similar firing patterns to the N1Ls, but where the frequency of the rhythm depends on the level of injected current. 4. The N1Ls' ability to drive a fictive feeding rhythm in the isolated preparation was due to their strong, monosynaptic excitatory chemical connection with the N1M CPG interneurons. Bursts of spikes in the N1Ls generated summating excitatory postsynaptic potentials (EPSPs) in the N1Ms to drive them to firing. The SO excited the N1M cells in a similar way, but the EPSPs are strongly facilitatory, unlike the N1L-->N1M connection. 5. Fast (1 cycle every 5 s) fictive feeding rhythms driven by the N1L occurred in the absence of spike activity in the SO modulatory neuron. In contrast, the N1L was usually active in SO-driven rhythms. 6. The ability of the SO to drive the N1L was due to strong electrotonic coupling, SO-->N1L. The weaker coupling in the opposite direction, N1L-->SO, did not allow the N1L to drive the SO. 7. Experiments on semintact lip-brain preparations allowed fictive feeding to be evoked by application of 0.1 M sucrose to the lips (mimicking the normal sensory input) rather than by injection of depolarizing current. Rhythmic bursting, characteristic of fictive feeding, began in both the SO and N1L at exactly the same time, indicating that these two cell types are activated in "parallel" to drive the feeding rhythm. 8. The N1L is also part of the CPG network. It Excited the N2s and inhibited the N3 phasic (N3p) and N3 tonic (N3t) CPG interneurons like the N1Ms.(ABSTRACT TRUNCATED AT 400 WORDS)


2007 ◽  
Vol 70 (10-12) ◽  
pp. 1797-1801 ◽  
Author(s):  
Roberto Latorre ◽  
Francisco de Borja Rodríguez ◽  
Pablo Varona

2000 ◽  
Vol 83 (2) ◽  
pp. 879-887 ◽  
Author(s):  
Krešimir Krnjević ◽  
Yong-Tao Zhao

In previous experiments on excitatory synaptic transmission in CA1, temporary (10–20 min) replacement of glucose with 10 mM 2-deoxyglucose (2-DG) consistently caused a marked and very sustained potentiation (2-DG LTP). To find out whether 2-DG has a similar effect on inhibitory synapses, we recorded pharmacologically isolated mononosynaptic inhibitory postsynaptic potentials (IPSPs; under current clamp) and inhibitory postsynaptic currents (IPSCs; under voltage clamp); 2-DG was applied both in the presence and the absence of antagonists of N-methyl-d-aspartate (NMDA). In spite of sharply varied results (some neurons showing large potentiation, lasting for >1 h, and many little or none), overall there was a significant and similar potentiation of IPSP conductance, both for the early (at ≈30 ms) and later (at ≈140 ms) components of IPSPs or IPSCs: by 35.1 ± 10.25% (mean ± SE; for n = 24, P = 0.0023) and 36.5 ± 16.3% (for n = 19, P = 0.038), respectively. The similar potentiation of the early and late IPSP points to a presynaptic mechanism of LTP. Overall, the LTP was statistically significant only when 2-DG was applied in the absence of glutamate antagonists. Tetanic stimulations (in presence or absence of glutamate antagonists) only depressed IPSPs (by half). In conclusion, although smaller and more variable, 2-DG–induced LTP of inhibitory synapses appears to be broadly similar to the 2-DG–induced LTP of excitatory postsynaptic potentials previously observed in CA1.


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.


1983 ◽  
Vol 55 (6) ◽  
pp. 1647-1659 ◽  
Author(s):  
C. von Euler

Recent advances in several laboratories concerning the respiration-related medullary neurons, their locations, projections, interconnections, morphological and physiological properties, and patterns of inhibitory postsynaptic potentials, excitatory postsynaptic potentials, and discharge rate, on the one hand, and the “systems behavior,” on the other, have provided the basis for new hypothesis concerning the neural mechanisms underlying the central pattern generator (CPG) for breathing and its different parts. The onset of the “ramp”-like increase in inspiratory activity is due to an abrupt release of inhibition and a subsequent progressively increasing synaptic excitation of inspiratory premotor neurons. The integration of the excitatory “drive” inputs underlying the ramp inspiratory activity seems to depend on structures in the ventrorostral medulla, including nucleus paragigantocellularis. The termination of this activity by the off-switch mechanisms is actuated when a critical threshold is attained by the excitatory inputs of 1) a slowly increasing inspiration-related activity and 2) the afferent input from the pulmonary stretch receptors. The nature of the former activity is discussed. During the expiratory phase, an inhibitory activity suppresses inspiration-facilitating inputs with a slowly decaying power that controls the expiratory duration. The postinspiration activity, which brakes the rate of exhalation during the first part of the expiratory phase, depends on mechanisms separate from those responsible for the inspiratory ramp activity. The respiratory CPG seems to be organized with considerable amount of redundancy, or “degeneracity.”


2013 ◽  
Vol 109 (10) ◽  
pp. 2451-2465 ◽  
Author(s):  
Alex H. Williams ◽  
Molly A. Kwiatkowski ◽  
Adam L. Mortimer ◽  
Eve Marder ◽  
Mary Lou Zeeman ◽  
...  

The cardiac ganglion (CG) of Homarus americanus is a central pattern generator that consists of two oscillatory groups of neurons: “small cells” (SCs) and “large cells” (LCs). We have shown that SCs and LCs begin their bursts nearly simultaneously but end their bursts at variable phases. This variability contrasts with many other central pattern generator systems in which phase is well maintained. To determine both the consequences of this variability and how CG phasing is controlled, we modeled the CG as a pair of Morris-Lecar oscillators coupled by electrical and excitatory synapses and constructed a database of 15,000 simulated networks using random parameter sets. These simulations, like our experimental results, displayed variable phase relationships, with the bursts beginning together but ending at variable phases. The model suggests that the variable phasing of the pattern has important implications for the functional role of the excitatory synapses. In networks in which the two oscillators had similar duty cycles, the excitatory coupling functioned to increase cycle frequency. In networks with disparate duty cycles, it functioned to decrease network frequency. Overall, we suggest that the phasing of the CG may vary without compromising appropriate motor output and that this variability may critically determine how the network behaves in response to manipulations.


1979 ◽  
Vol 82 (1) ◽  
pp. 163-176
Author(s):  
RONALD L. CALABRESE

1. Inhibitory synapses among the central neurones involved in the generation of the heartbeat rhythm of the leech were blocked by either low Cl− physiological saline or presynaptic hyperpolarizing current. 2. Low Cl− saline reversibly blocked inhibitory postsynaptic potentials (IPSPs) from the HN cells onto both other HN cells and HE cells but did not block electrical coupling among HN cells. 3. The rhythmic bursts of impulses in HE cells were abolished when IPSPs were blocked by either low Cl− saline or hyperpolarization of HN cells. 4. The rhythmic bursts of impulses in HN cells were not abolished (except in cell HN(5)) when IPSPs were blocked by low Cl− saline, but phase relations became unfixed (unless the cells were electrically coupled). 5. Both brief depolarizing and hyperpolarizing current pulses reset the rhythm of HN cells whose IPSPs were blocked by low Cl− saline. 6. The results indicate that the motor neurones to the heart (HE cells) produce rhythmic impulse bursts because their steady discharge is periodically inhibited by the HN interneurones. The pattern generated by the HN cells originates from an endogenous rhythm co-ordinated by the inhibitory interactions and electrical coupling between these cells.


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