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.

Glutamate is the Transmitter for N2v Retraction Phase Interneurons of the Lymnaea Feeding System

1997 ◽  
Vol 78 (6) ◽  
pp. 3408-3414 ◽  
Author(s):  
M. J. Brierley ◽  
M. S. Yeoman ◽  
P. R. Benjamin
Keyword(s):  
Nmda Receptors ◽  
Glutamate Receptor ◽  
Motor Neurons ◽  
Nmda Receptor Antagonist ◽  
Receptor Subtype ◽  
Feeding System ◽  
Cell Responses ◽  
Bath Application ◽  
Strong Candidate

Brierley, Matthew J., Mark S. Yeoman, and Paul R. Benjamin. Glutamate is the transmitter for the N2v retraction phase interneurons of the Lymnaea feeding system. J. Neurophysiol. 78: 3408–3414, 1997. Electrophysiological and pharmacological methods were used to examine the role of glutamate in mediating the excitatory and inhibitory responses produced by the N2v rasp phase neurons on postsynaptic cells of the Lymnaea feeding network. The N2v → B3 motor neuron excitatory synaptic response could be mimicked by focal or bath application of l-glutamate at concentrations of ≥10−3 M. Quisqualate and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) were potent agonists for the B3 excitatory glutamate receptor (10−3 M), whereas kainate only produced very weak responses at the same concentration. This suggested that non- N-methyl-d-aspartate (NMDA), AMPA/quisqualate receptors were present on the B3 cell. The specific non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 10−5 M) blocked 85% of the excitatory effects on the B3 cell produced by focal application of glutamate (10−3 M), confirming the presence of non-NMDA receptors. CNQX also blocked the major part of the excitatory postsynaptic potentials on the B3 cell produced by spontaneous or current-evoked bursts of spikes in the N2v cell. As with focal application of glutamate, a small delayed component remained that was CNQX insensitive. This provided direct evidence that glutamate acting via receptors of the non-NMDA, AMPA/quisqualate type were responsible for mediating the main N2v → B3 cell excitatory response. NMDA at 10−2 M also excited the B3 cell, but the effects were much more variable in size and absent in one-third of the 25 B3 cells tested. NMDA effects on B3 cells were not enhanced by bath application of glycine at 10−4 M or reduction of Mg2+ concentration in the saline to zero, suggesting the absence of typical NMDA receptors. The variability of the B3 cell responses to NMDA suggested these receptors were unlikely to be the main receptor type involved with N2v → B3 excitation. Quisqualate and AMPA at 10−3 M also mimicked N2v inhibitory effects on the B7 and B8 feeding motor neurons and the modulatory slow oscillator (SO) interneuron, providing further evidence for the role of AMPA/quisqualate receptors. Similar effects were seen with glutamate at the same concentration. However, CNQX could not block either glutamate or N2v inhibitory postsynaptic responses on the B7, B8, or SO cells, suggesting a different glutamate receptor subtype for inhibitory responses compared with those responsible for N2v → B3 excitation. We conclude that glutamate is a strong candidate transmitter for the N2v cells and that AMPA/quisquate receptors of different subtypes are likely to be responsible for the excitatory and inhibitory postsynaptic responses.

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.

Synaptic relationships of the cerebral giant cells with motoneurones in the feeding system of Lymnaea stagnalis

1980 ◽  
Vol 85 (1) ◽  
pp. 169-186
Author(s):  
C. R. McCrohan ◽  
P. R. Benjamin
Keyword(s):  
Synaptic Input ◽  
Lymnaea Stagnalis ◽  
Giant Cells ◽  
Burst Activity ◽  
Feeding System ◽  
Postsynaptic Potentials ◽  
Buccal Ganglia ◽  
Long Latency ◽  
Burst Intensity ◽  
Feeding Cycle

1.The cerebral giant cells (CGCs) of Lymnaea have a tonic, modulatory effect on the intensity of output from feeding motoneurones in the buccal ganglia. 2. Short latency, excitatory and probably monosynaptic connexions occur between the CGCs and three identified feeding motoneurones. Unitary excitatory postsynaptic potentials in these motoneurones, following CGC spikes, are of different sizes and durations, and hence have different summation properties. 3. The CGCs make long latency, excitatory polysynaptic connexions with four other feeding motoneurone types. 4. Bursts of spikes in the CGCs, resulting from phasic synaptic input, synchronous with the feeding cycle, amplify their modulatory effect on burst intensity in feeding motoneurones. 5. Thte for reinforcing their cyclic burst activity.

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.

Role of chloride-homeostasis in the inhibitory control of neuronal network oscillators

1996 ◽  
Vol 75 (6) ◽  
pp. 2654-2657 ◽  
Author(s):  
W. Jarolimek ◽  
H. Brunner ◽  
A. Lewen ◽  
U. Misgeld
Keyword(s):  
Glycine Receptor ◽  
Membrane Conductance ◽  
Burst Activity ◽  
Synaptic Activity ◽  
Gamma Aminobutyric Acid ◽  
Chloride Homeostasis ◽  
Outward Transport ◽  
Whole Cell Recordings ◽  
Rhythmic Burst

1. Spontaneous synaptic activity in networks formed by dissociated neurons from embryonic rat midbrain was analyzed in tight seal whole cell recordings. 2. Application of furosemide (0.5 mM) to the cell and its surrounding area increased the frequency of spontaneous synaptic currents. Incubation of the culture with furosemide resulted in “rhythmic” burst activity. 3. Furosemide (0.1-0.5 mM) changed equilibrium potentials of inhibitory postsynaptic currents, gamma-aminobutyric acid-A (GABAA) or glycine receptor-mediated Cl- currents by a blockade of Cl(-)-outward transport. Furosemide did not alter the slope conductance of GABAA receptor-mediated currents. Membrane conductance and cell excitability were also unaffected. 4. We conclude that furosemide locked the activity of the network in “burst activity” mode through impairment of inhibition resulting from the disturbance of Cl- homeostasis.

Serotonergic modulation of locust motor neurons

1995 ◽  
Vol 73 (3) ◽  
pp. 923-932 ◽  
Author(s):  
D. Parker
Keyword(s):  
Cyclic Amp ◽  
Motor Neurons ◽  
Schistocerca Gregaria ◽  
Phosphodiesterase Inhibitor ◽  
Membrane Resistance ◽  
Excitatory Postsynaptic Potential ◽  
Metathoracic Ganglion ◽  
Bath Application ◽  
Potassium Conductances ◽  
5 Ht Uptake

1. The effects of the putative endogenous neuromodulator serotonin (5-HT) on the fast extensor and flexor tibiae motor neurons in the locust (Schistocerca gregaria) metathoracic ganglion, were analyzed. 2. 5-HT consistently increased the duration of the fast extensor spike and usually reduced the afterhyperpolarization, although this effect was less consistent. The spike broadening in the fast extensor was associated with an increase in the amplitude of the excitatory postsynaptic potential (EPSP) evoked monosynaptically in the flexor motor neurons by fast extensor stimulation. 5-HT also increased the membrane resistance of the fast extensor and flexor tibiae motor neurons. 3. The effects of 5-HT were mimicked by bath application of the 5-HT uptake inhibitor imipramine, and blocked by the 5-HT receptor antagonist ketanserin. The effects were also mimicked by dibutryl cyclic AMP, a membrane permeant analogue of cyclic AMP, and by the phosphodiesterase inhibitor 3-isobutyl-1-methyl-xanthine, but not by dibutryl cyclic GMP. The 5-HT-dependent modulation was blocked by the protein kinase A inhibitor H8. In addition, injection of cyclic AMP into the fast extensor or a flexor motor neuron could mimic the effects of 5-HT on these neurons. 4. 5-HT probably broadened the FETi action potential by modulating potassium conductances responsible for spike repolarization. 5. These results show that 5-HT modulates both the fast extensor and flexor tibiae motor neurons, resulting in potentiation of synaptic transmission between these neurons. In addition, the increase in flexor membrane resistance will potentiate other inputs onto these cells, which will affect the output of the motor neurons during locomotion.

Analysis of decreased conductance serotonergic response in Aplysia ink motor neurons

1985 ◽  
Vol 53 (2) ◽  
pp. 590-602 ◽  
Author(s):  
J. P. Walsh ◽  
J. H. Byrne
Keyword(s):  
Cell Body ◽  
Motor Neurons ◽  
Potassium Conductance ◽  
Membrane Conductance ◽  
Resting Potential ◽  
Slow Inward Current ◽  
Equilibrium Potential ◽  
Voltage Sensitivity ◽  
Inward Current ◽  
Bath Application

Micropressure ejection of serotonin (5-hydroxytryptamine, 5-HT) produced excitatory responses in the L14 ink motor neurons of Aplysia that depended on the site of application. Ejection of 5-HT onto the cell body produced a slow response that showed variability in voltage sensitivity between preparations. In contrast, ejection of 5-HT onto the neuropil underneath the cell body produced a response whose amplitude was consistently a linear function of the holding potential, reversing near the predicted potassium equilibrium potential. Subsequent analyses focused on this second response. The neuropil response induced by 5-HT had a linear current-voltage relationship (reversing at ca. -80 mV), was associated with a decrease in input conductance, and was sensitive to changes in the concentration of extracellular K+. Serotonin application in artificial seawater (ASW) containing 30 mM K+ produced a response that reversed close to the altered Nernst potential for K+. The 5-HT response did not appear to be due to secondary activation of interneurons or to depend primarily on extracellular Ca2+, since ejection of 5-HT onto cells bathed in ASW containing 30 mM Co2+ produced responses comparable to, although somewhat attenuated from, those observed in ASW. Serotonin responses similar to those produced in ASW were obtained after perfusing the ganglion with ASW containing Co2+, 4-aminopyridine (4-AP), and tetraethylammonium (TEA). This suggests that the 5-HT-sensitive current is separate from the Ca2+-activated, fast, and delayed rectifying K+ currents. The 5-HT response appeared to be mediated by changes in levels of cAMP. Bath application of the phosphodiesterase inhibitors IBMX (3-isobutyl-1-methylxanthine) or Ro 20-1724, or the adenylate cyclase activator forskolin mimicked the 5-HT response by producing a slow inward current associated with a decrease in membrane conductance. Alteration of cellular cAMP metabolism modulated the response to 5-HT. Exposure of the ganglion to low concentrations of either Ro 20-1724 or forskolin potentiated the 5-HT response. Higher concentrations of these agents largely blocked the response to subsequent 5-HT applications. Bath application of the 8-bromo derivative of either cAMP or cGMP produced a slow inward current associated with a decrease in membrane conductance in cells voltage clamped at the resting potential. Responses to 5-HT were blocked, however, after exposure to 8-bromo-cAMP, but not to 8-bromo-cGMP. These results suggest that 5-HT produces a voltage-independent decrease in a steady-state potassium conductance that may be mediated by cAMP.(ABSTRACT TRUNCATED AT 400 WORDS)

Endogenous Motor Neuron Properties Contribute to a Program-Specific Phase of Activity in the Multifunctional Feeding Central Pattern Generator of Aplysia

2007 ◽  
Vol 98 (1) ◽  
pp. 29-42 ◽  
Author(s):  
Geidy E. Serrano ◽  
Clarissa Martínez-Rubio ◽  
Mark W. Miller
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Central Pattern Generators ◽  
Ingestive Behavior ◽  
Membrane Properties ◽  
Motor Patterns ◽  
Effector System ◽  
Bilateral Pair ◽  
Pattern Generators ◽  
Specific Phase

Multifunctional central pattern generators (CPGs) are circuits of neurons that can generate manifold actions from a single effector system. This study examined a bilateral pair of pharyngeal motor neurons, designated B67, that participate in the multifunctional feeding network of Aplysia californica. Fictive buccal motor programs (BMPs) were elicited with four distinct stimulus paradigms to assess the activity of B67 during ingestive versus egestive patterns. In both classes of programs, B67 fired during the phase of radula protraction and received a potent inhibitory postsynaptic potential (IPSP) during fictive radula retraction. When programs were ingestive, the retraction phase IPSP exhibited a depolarizing sag and was followed by a postinhibitory rebound (PIR) that could generate a postretraction phase of impulse activity. When programs were egestive, the depolarizing sag potential and PIR were both diminished or were not present. Examination of the membrane properties of B67 disclosed a cesium-sensitive depolarizing sag, a corresponding Ih-like current, and PIR in its responses to hyperpolarizing pulses. Direct IPSPs originating from the influential CPG retraction phase interneuron B64 were also found to activate the sag potential and PIR of B67. Dopamine, a modulator that can promote ingestive behavior in this system, enhanced the sag potential, Ih-like current, and PIR of B67. Finally, a pharyngeal muscle contraction followed the radula retraction phase of ingestive, but not egestive motor patterns. It is proposed that regulation of the intrinsic properties of this motor neuron can contribute to generating a program-specific phase of motor activity.

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.

Sign in / Sign up

Export Citation Format

Share Document