Different Roles of Neurons B63 and B34 That Are Active During the Protraction Phase of Buccal Motor Programs in Aplysia californica

1997 ◽  
Vol 78 (3) ◽  
pp. 1305-1319 ◽  
Author(s):  
Itay Hurwitz ◽  
Irving Kupfermann ◽  
Abraham J. Susswein
Keyword(s):  
Motor Neurons ◽  
Aplysia Californica ◽  
Motor Program ◽  
Excitatory Postsynaptic Potential ◽  
Strongly Correlated ◽  
Excitatory Effect ◽  
Buccal Ganglion ◽  
Motor Programs ◽  
Pattern Characteristic ◽  
Protraction Phase

Hurwitz, Itay, Irving Kupfermann, and Abraham J. Susswein. Different roles of neurons B63 and B34 that are active during the protraction phase of buccal motor programs in Aplysia californica. J. Neurophysiol. 78: 1305–1319, 1997. The buccal ganglion of Aplysia contains a central pattern generator (CPG) that organizes sequences of radula protraction and retraction during food ingestion and egestion. Neurons B63 and B34 have access to, or are elements of, the CPG. Both neurons are depolarized along with B31/B32 during the protraction phase of buccal motor programs. Both cells excite the contralateral B31/B32 neurons and inhibit B64 and other neurons active during the retraction phase. B63 and B34 also both have an axon exiting the buccal ganglia via the contralateral cerebrobuccal connective. Despite their similarities, B63 and B34 differ in a number of properties, which reflects their different functions. B63 fires during both ingestion and egestion-like buccal motor programs, whereas B34 fires only during egestion-like programs. The bilateral B63 neurons, along with the bilateral B31 and B32 neurons, act as a single functional unit. Sufficient depolarization of any of these neurons activates them all and initiates a buccal motor program. B63 is electrically coupled to both the ipsilateral and the contralateral B31/B32 neurons but monosynaptically excites the contralateral neurons with a mixed electrical and chemical excitatory postsynaptic potential (EPSP). Positive feedback caused by electrical and chemical EPSPs between B63 and B31/B32 contributes to the sustained depolarization in B31/B32 and the firing of B63 during the protraction phase of a buccal motor program. B34 is excited during the protraction phase of all buccal motor programs, but, unlike B63, it does not always reach firing threshold. The neuron fires in response to current injection only after it is depolarized for 1–2 s or after preceding buccal motor programs in which it is depolarized. Firing of B34 produces facilitating EPSPs in the contralateral B31/B32 and B63 neurons and can initiate a buccal motor program. Firing in B34 is strongly correlated with firing in the B61/B62 motor neurons, which innervate the muscle (I2) responsible for much of protraction. B34 monosynaptically excites these motor neurons. B34 firing is also correlated with firing in motor neuron B8 during the protraction phase of a buccal motor program. B8 innervates the I4 radula closer muscle, which in egestion movements is active during protraction and in ingestion movements is active during retraction. B34 has a mixed, but predominantly excitatory, effect on B8 via a slow conductance-decrease EPSP. Thus firing in B34 leads to amplification of radula protraction that is coupled with radula closing, a pattern characteristic of egestion.

scholarly journals Release of a single neurotransmitter from an identified interneuron coherently affects motor output on multiple time scales

2013 ◽  
Vol 109 (9) ◽  
pp. 2327-2334 ◽  
Author(s):  
Andrew M. Dacks ◽  
Klaudiusz R. Weiss
Keyword(s):  
Time Scales ◽  
Motor Program ◽  
Gaba Release ◽  
Motor Output ◽  
Multiple Time Scales ◽  
Multiple Time ◽  
Intrinsic Properties ◽  
Buccal Ganglion ◽  
Motor Programs ◽  
Pattern Characteristic

Neurotransmitters can have diverse effects that occur over multiple time scales often making the consequences of neurotransmission difficult to predict. To explore the consequences of this diversity, we used the buccal ganglion of Aplysia to examine the effects of GABA release by a single interneuron, B40, on the intrinsic properties and motor output of the radula closure neuron B8. B40 induces a picrotoxin-sensitive fast IPSP lasting milliseconds in B8 and a slow EPSP lasting seconds. We found that the excitatory effects of this slow EPSP are also mediated by GABA. Together, these two GABAergic actions structure B8 firing in a pattern characteristic of ingestive programs. Furthermore, we found that repeated B40 stimulation induces a persistent increase in B8 excitability that was occluded in the presence of the GABA B receptor agonist baclofen, suggesting that GABA affects B8 excitability over multiple time scales. The phasing of B8 activity during the feeding motor programs determines the nature of the behavior elicited during that motor program. The persistent increase in B8 excitability induced by B40 biased the activity of B8 during feeding motor programs causing the motor programs to become more ingestive in nature. Thus, a single transmitter released from a single interneuron can have consequences for motor output that are expressed over multiple time scales. Importantly, despite the differences in their signs and temporal characteristics, the three actions of B40 are coherent in that they promote B8 firing patterns that are characteristic of ingestive motor outputs.

B64, a newly identified central pattern generator element producing a phase switch from protraction to retraction in buccal motor programs of Aplysia californica

1996 ◽  
Vol 75 (4) ◽  
pp. 1327-1344 ◽  
Author(s):  
I. Hurwitz ◽  
A. J. Susswein
Keyword(s):  
Phase Shift ◽  
Central Pattern Generator ◽  
Motor Program ◽  
Pattern Generator ◽  
Synaptic Activity ◽  
Excitatory Postsynaptic Potential ◽  
Motor Programs ◽  
Identified Neuron ◽  
Protraction Phase ◽  
Two Phases

1. Buccal motor programs in Aplysia are characterized by two phases of activity, which represent protraction and retraction of the radula in intact animals. The shift from protraction to retraction is caused by synaptic activity inhibiting neurons that are active during protraction and exciting neurons that are active during retraction. 2. B64, a newly identified neuron present bilaterally in the buccal ganglia, is partially responsible for the phase shift. Stimulating a single B64 causes bilateral inhibition of neurons B31/B32 and other neurons active during protraction and cause bilateral excitation of neurons B4/B5 and other neurons active during retraction. B64 is active throughout retraction. The amplitude and waveforms of the synaptic potentials caused by firing B64 are similar, but not identical, to those seen during retraction. 3. Some of the effects of B64 on B31/B32 and on B4/B5 are monosynaptic, as shown by their maintained presence in high divalent cation seawater, which blocks polysynaptic activity. 4. A brief depolarization of B64 leads to a long-lasting depolarization and firing. The ability of B64 to respond in this way is at least partially caused by an endogenous plateau potential, as this property is still seen after synaptic transmission is blocked. 5. Hyperpolarization of B64 bilaterally and preventing the somata from firing unmasks a large excitatory postsynaptic potential in B64. This procedure does not block the shift from protraction to retraction, indicating that spiking in the B64 somata is not necessary for the phase shift. 6. The firing pattern and synaptic connections of B64 are consistent with the hypothesis that the neuron is part of a central pattern generator underlying buccal motor programs. B64 is monosynaptically inhibited by neurons that are active along with B31/B32, which are responsible for producing the protraction phase of a buccal motor program. During the later portion of the protraction phase B64 is excited. In addition, firing B64 can phase advance and phase delay buccal motor programs. 7. Regulating the firing of B64 can regulate the expression of buccal motor programs. Stimulation of B64 at frequencies of 0.5-1.0 Hz leads to complete inhibition of buccal motor programs, whereas steady-state depolarization of B64 can lead to repetitive bursts of activity.

Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica

1996 ◽  
Vol 75 (4) ◽  
pp. 1309-1326 ◽  
Author(s):  
I. Hurwitz ◽  
D. Neustadter ◽  
D. W. Morton ◽  
H. J. Chiel ◽  
A. J. Susswein
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Activity Patterns ◽  
Aplysia Californica ◽  
Motor Programs ◽  
Physiological Functions ◽  
Rest Position ◽  
Buccal Ganglia ◽  
Normal Feeding ◽  
Protraction Phase

1. B31 and B32 are pattern-initiator neurons in the buccal ganglia of Aplysia. Along with the B61/B62 neurons, B31/B32 are also motor neurons that innervate the 12 buccal muscle via the I2 nerve. This research was aimed at determining the physiological functions of the B31/B32 and B61/B62 neurons, and of the I2 muscle. 2. Stimulating the I2 muscle in the radula rest position produces radula protraction. In addition, in behaving animals lesioning either the muscle or the I2 nerve greatly reduces radula protraction. 3. During buccal motor programs in reduced preparations, B31/B32 and B61/62 fire preceding activity in neuron B4, whose firing indicates the onset of radula retraction. In addition, during both ingestion-like and rejection-like patterns the activity in the I2 nerve is correlated with protraction. 4. B31/B32 fire at frequencies of 15-25 Hz. Neither B31/B32 nor B61/B62 elicit facilitating end-junction potentials (EJPs) and electromyograms (EMGs) in the I2 muscle. EMGs from B31/B32 are smaller than those from B61/B62. B31/B32 and B61/B62 innervate all areas of the muscle approximately uniformly. 5. In behaving animals, EMGs consistent with B31/B32 activity are seen in the I2 muscle during the protraction phase of biting, swallowing, and rejection movements. In addition, the I2 muscle receives inputs that cannot be attributed to either the B31/B32 or B61/B62 neurons, either because the potentials are too large, firing frequencies are too low, or a prominent facilitation is seen. Such potentials are associated with lip movements, and also with radula retraction. 6. EMGs were recorded from the I2 muscle during feeding behavior after a lesion of the I2 nerve. Animals that had severe deficits in protraction showed no activity consistent with B31/B32 or B61/B62, but did show activity during retraction. 7. Our data indicate that the I2 muscle and the B31/B32 motor neurons are essential constituents contributing to protraction movements. Activity in these neurons is associated with radula protraction, which occurs as a component of a number of different feeding movements. The I2 muscle may also contribute to retraction, via activation by other motor neurons.

scholarly journals Functional Genetic Screen to Identify Interneurons Governing Behaviorally Distinct Aspects of Drosophila Larval Motor Programs

2016 ◽  
Author(s):  
Matt Q. Clark ◽  
Stephanie J. McCumsey ◽  
Sereno Lopez-Darwin ◽  
Ellie S. Heckscher ◽  
Chris Q. Doe
Keyword(s):  
Motor Neurons ◽  
Animal Behavior ◽  
Motor Program ◽  
Genetic Screen ◽  
Muscle Contractions ◽  
Specific Expression ◽  
Motor Programs ◽  
Secondary Screen ◽  
Forward Locomotion ◽  
Sparse Pattern

AbstractDrosophila larval crawling is an attractive system to study patterned motor output at the level of animal behavior. Larval crawling consists of waves of muscle contractions generating forward or reverse locomotion. In addition, larvae undergo additional behaviors including head casts, turning, and feeding. It is likely that some neurons are used in all these behaviors (e.g. motor neurons), but the identity (or even existence) of neurons dedicated to specific aspects of behavior is unclear. To identify neurons that regulate specific aspects of larval locomotion, we performed a genetic screen to identify neurons that, when activated, could elicit distinct motor programs. We used 165 Janelia CRM-Gal4 lines – chosen for sparse neuronal expression – to express the warmth-inducible neuronal activator TrpA1 and screened for locomotor defects. The primary screen measured forward locomotion velocity, and we identified 63 lines that had locomotion velocities significantly slower than controls following TrpA1 activation (28°C). A secondary screen was performed on these lines, revealing multiple discrete behavioral phenotypes including slow forward locomotion, excessive reverse locomotion, excessive turning, excessive feeding, immobile, rigid paralysis, and delayed paralysis. While many of the Gal4 lines had motor, sensory, or muscle expression that may account for some or all of the phenotype, some lines showed specific expression in a sparse pattern of interneurons. Our results show that distinct motor programs utilize distinct subsets of interneurons, and provide an entry point for characterizing interneurons governing different elements of the larval motor program.

Intrinsic and Extrinsic Modulation of a Single Central Pattern Generating Circuit

2000 ◽  
Vol 84 (3) ◽  
pp. 1186-1193 ◽  
Author(s):  
Peter T. Morgan ◽  
Ray Perrins ◽  
Philip E. Lloyd ◽  
Klaudiusz R. Weiss
Keyword(s):  
Neural Circuits ◽  
Central Pattern Generators ◽  
Motor Program ◽  
Pattern Generator ◽  
Motor Programs ◽  
Appetitive Behavior ◽  
Protraction Phase ◽  
Pattern Generators ◽  
Rhythmic Behaviors ◽  
Appetitive Behaviors

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.

Afferent-Induced Changes in Rhythmic Motor Programs in the Feeding Circuitry of Aplysia

2004 ◽  
Vol 92 (4) ◽  
pp. 2312-2322 ◽  
Author(s):  
Avniel N. Shetreat-Klein ◽  
Elizabeth C. Cropper
Keyword(s):  
Sensory Neurons ◽  
Motor Neurons ◽  
Rhythmic Activity ◽  
Motor Program ◽  
Firing Frequency ◽  
Afferent Activity ◽  
Motor Programs ◽  
Rhythmic Motor ◽  
Induced Changes ◽  
The Impact

A manipulation often used to determine whether a neuron plays a role in the generation of a motor program involves injecting current into the cell during rhythmic activity to determine whether activity is modified. We perform this type of manipulation to study the impact of afferent activity on feeding-like motor programs in Aplysia. We trigger biting-like programs and manipulate sensory neurons that have been implicated in producing the changes in activity that occur when food is ingested, i.e., when bites are converted to bite-swallows. Sensory neurons that are manipulated are the radula mechanoafferent B21 and the retraction proprioceptor B51. Data suggest that both cells are peripherally activated during radula closing/retraction when food is ingested. We found that phasic subthreshold depolarization of a single sensory neuron can significantly prolong radula closing/retraction, as determined by recording both from interneurons (e.g., B64), and motor neurons (e.g., B15 and B8). Additionally, afferent activity produces a delay in the onset of the subsequent radula opening/protraction, and increases the firing frequency of motor neurons. These are the changes in activity that are seen when food is ingested. These results add to the growing data that implicate B21 and B51 in bite to bite-swallow conversions and indicate that afferent activity is important during feeding in Aplysia.

Depression of synaptic connections between identified motor neurons in the locust

1995 ◽  
Vol 74 (2) ◽  
pp. 529-538 ◽  
Author(s):  
D. Parker
Keyword(s):  
Action Potential ◽  
Motor Neuron ◽  
Motor Neurons ◽  
Motor Program ◽  
Excitatory Postsynaptic Potential ◽  
Epsp Amplitude ◽  
Spike Amplitude ◽  
Posterior Group ◽  
High Calcium ◽  
Frequency Stimulation

1. The fast extensor tibiae motor neuron makes direct excitatory central connections with the posterior group of flexor tibiae motor neurons in the locust metathoracic ganglion. The flexor group has a slow, a fast, and an intermediate motor neuron. The motor neurons are involved in the motor program for kicking and jumping, the defensive and escape behaviors of the locust. An antidromic action potential in fast extensor tibiae motor neuron (FETi) results in a monosynaptic, glutamatergic excitatory postsynaptic potential (EPSP) in each of the flexor motor neurons. 2. A train of 10 antidromic spikes in FETi at frequencies of 1<20 Hz resulted in depression of the amplitude of the EPSP in each of the flexor motor neurons. The depression was not significantly different in the different flexor motor neurons. The depression was greater with higher frequency stimulation and was reduced in low calcium saline. 3. After stimulation at 20 Hz, the EPSP amplitude was depressed by approximately 80%. This did not change when the number of stimuli was increased to 20, when stimulation was done in high calcium saline, or when the frequency of stimulation was increased to 50 or 100 Hz. The recovery from depression was greater after 20-Hz stimulation than at lower frequencies, although the recovery was reduced when the number of stimuli was increased, and also in high calcium saline. 4. In normal saline the depression of the EPSP amplitude was associated with a reduction of the presynaptic spike amplitude at frequencies of > or = 5 Hz. In tetraethylammonium (TEA) saline the width of a TEA-broadened spike was also reduced. The reduction in spike amplitude and spike width correlated with the depression of the EPSP. 5. Certain of these results are consistent with a depletion model of synaptic depression, whereas others are not consistent with this model. The depression may be partly due to an initial depletion of transmitter stores, and partly to modulation of the presynaptic action potential that reduces calcium entry, and therefore transmitter release. The significance of the depression on the motor program for kicking and jumping is discussed.

Feeding CPG in Aplysia Directly Controls Two Distinct Outputs of a Compartmentalized Interneuron That Functions as a CPG Element

2007 ◽  
Vol 98 (6) ◽  
pp. 3796-3801 ◽  
Author(s):  
Kosei Sasaki ◽  
Michael R. Due ◽  
Jian Jing ◽  
Klaudiusz R. Weiss
Keyword(s):  
Action Potentials ◽  
Electrical Coupling ◽  
Motor Program ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Buccal Ganglion ◽  
Full Size ◽  
Program Generation ◽  
Functional Aspects ◽  
Protraction Phase

In the context of motor program generation in Aplysia, we characterize several functional aspects of intraneuronal compartmentalization in an interganglionic interneuron, CBI-5/6. CBI-5/6 was shown previously to have a cerebral compartment (CC) that includes a soma that does not generate full-size action potentials and a buccal compartment (BC) that does. We find that the synaptic connections made by the BC of CBI-5/6 in the buccal ganglion counter the activity of protraction-phase neurons and reinforce the activity of retraction-phase neurons. In buccal motor programs, the BC of CBI-5/6 fires phasically, and its premature activation can phase advance protraction termination and retraction initiation. Thus the BC of CBI-5/6 can act as an element of the central pattern generator (CPG). During protraction, the CC of CBI-5/6 receives direct excitatory inputs from the CPG elements, B34 and B63, and during retraction, it receives antidromically propagating action potentials that originate in the BC of CBI-5/6. Consequently, in its CC, CBI-5/6 receives depolarizing inputs during both protraction and retraction, and these depolarizations can be transmitted via electrical coupling to other neurons. In contrast, in its BC, CBI-5/6 uses spike-dependent synaptic transmission. Thus the CPG directly and differentially controls the program phases in which the two compartments of CBI-5/6 may transmit information to its targets.

Food avoidance learning is accompanied by synaptic attenuation in identified interneurons controlling feeding behavior in Pleurobranchaea

1986 ◽  
Vol 56 (3) ◽  
pp. 891-905 ◽  
Author(s):  
M. P. Kovac ◽  
E. M. Matera ◽  
P. J. Volk ◽  
W. J. Davis
Keyword(s):  
Motor Program ◽  
Corollary Discharge ◽  
Identified Neurons ◽  
Excitatory Postsynaptic Potential ◽  
Buccal Ganglion ◽  
Food Avoidance ◽  
The Mean ◽  
Necessary And Sufficient ◽  
Induced Changes ◽  
The Brain

Identified paracerebral feeding command interneurons (PCNs) in the brain of the mollusc Pleurobranchaea excite other identified PCNs by means of a chemical polysynaptic pathway whose efficacy is reduced by food avoidance training (conditionally paired food and electric shock). The purpose of the present study was to identify the neurons comprising this pathway and to localize learning-induced changes to single identified neurons. We found that associative training strongly attenuates or abolishes a unitary excitatory postsynaptic potential (EPSP) at a single identified synapse in this polysynaptic pathway, but does not alter other synapses. The PCNs descend to the buccal ganglion, where they monosynaptically excite each member of a set of four identified neurons (two per hemiganglion) that belong to the corollary discharge population described previously. The strength of ascending and descending synapses involving identified PCNs is greatest ipsilaterally and is proportional to relative command efficacy established in previous studies. These findings suggest that command efficacy results directly from synaptic strength. The pair of corollary discharge neurons on each side of the buccal ganglion sends axons to the opposite side and thence up the contralateral cerebrobuccal connective to the brain. These neurons have therefore been termed the contralateral corollary discharge (CCD) neurons. Each CCD monosynaptically excites every PCN on both sides of the brain. Contralateral synaptic influences on identified PCNs are larger than ipsilateral ones. Each of the four identified CCD neurons is electrically coupled to all other members of the subset, including the contralateral homologue (based on simultaneous intracellular recording) and the ipsilateral partner (based on dye coupling). Hyperpolarizing a single CCD eliminates the polysynaptic response of PCNs to stimulation of other PCNs, whereas depolarizing a single CCD mimics the polysynaptic response. The CCD neurons are therefore necessary and sufficient to the polysynaptic response. Consistent with this role, the CCDs discharge in phase with the PCNs during the feeding motor program, and hyperpolarizing a CCD abolishes the cycle discharge of PCNs and weakens the feeding rhythm. Of the several reciprocal synapses identified between the PCNs and CCDs, only one was significantly altered by associative training in the food avoidance paradigm developed previously. This synapse, from the polysynaptic excitor (PSE) to the ipsilateral CCD, was also the strongest in this recurrent positive-feedback loop. In brains taken from conditioned specimens, the mean EPSP amplitude induced by a PSE action potential in ipsi

Cycle-to-Cycle Variability of Neuromuscular Activity in Aplysia Feeding Behavior

2004 ◽  
Vol 92 (1) ◽  
pp. 157-180 ◽  
Author(s):  
Charles C. Horn ◽  
Yuriy Zhurov ◽  
Irina V. Orekhova ◽  
Alex Proekt ◽  
Irving Kupfermann ◽  
...  
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Motor Program ◽  
Neuromuscular System ◽  
Motor Programs ◽  
Large Variability ◽  
Implanted Electrodes ◽  
Functional Behavior ◽  
High Level ◽  
Stimulation Of

Aplysia consummatory feeding behavior, a rhythmic cycling of biting, swallowing, and rejection movements, is often said to be stereotyped. Yet closer examination shows that cycles of the behavior are very variable. Here we have quantified and analyzed the variability at several complementary levels in the neuromuscular system. In reduced preparations, we recorded the motor programs produced by the central pattern generator, firing of the motor neurons B15 and B16, and contractions of the accessory radula closer (ARC) muscle while repetitive programs were elicited by stimulation of the esophageal nerve. In other similar experiments, we recorded firing of motor neuron B48 and contractions of the radula opener muscle. In intact animals, we implanted electrodes to record nerve or ARC muscle activity while the animals swallowed controlled strips of seaweed or fed freely. In all cases, we found large variability in all parameters examined. Some of this variability reflected systematic, slow, history-dependent changes in the character of the central motor programs. Even when these trends were factored out, however, by focusing only on the differences between successive cycles, considerable variability remained. This variability was apparently random. Nevertheless, it too was the product of central history dependency because regularizing merely the high-level timing of the programs also regularized many of the downstream neuromuscular parameters. Central motor program variability thus appears directly in the behavior. With regard to the production of functional behavior in any one cycle, the large variability may indicate broad tolerances in the operation of the neuromuscular system. Alternatively, some cycles of the behavior may be dysfunctional. Overall, the variability may be part of an optimal strategy of trial, error, and stabilization that the CNS adopts in an uncertain environment.

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