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.

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.

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.

Multiple Contributions of an Input-Representing Neuron to the Dynamics of the Aplysia Feeding Network

2007 ◽  
Vol 97 (4) ◽  
pp. 3046-3056 ◽  
Author(s):  
Alex Proekt ◽  
Jian Jing ◽  
Klaudiusz R. Weiss
Keyword(s):  
Central Pattern Generator ◽  
Motor Program ◽  
Pattern Generator ◽  
Higher Order ◽  
Motor Output ◽  
Slow Dynamics ◽  
Motor Programs ◽  
The Future

In Aplysia, mutually antagonistic ingestive and egestive behaviors are produced by the same multifunctional central pattern generator (CPG) circuit. Interestingly, higher-order inputs that activate the CPG do not directly specify whether the resulting motor program is ingestive or egestive because the slow dynamics of the network intervene. One input, the commandlike cerebral–buccal interneuron 2 (CBI-2), slowly drives the motor output toward ingestion, whereas another input, the esophageal nerve (EN), drives the motor output toward egestion. When the input is switched from EN to CBI-2, the motor output does not switch immediately and remains egestive. Here, we investigated how these slow dynamics are implemented on the interneuronal level. We found that activity of two CPG interneurons, B20 and B40, tracked the motor output regardless of the input, whereas activity of another CPG interneuron, B65, tracked the input regardless of the motor output. Furthermore, we show that the slow dynamics of the network are implemented, at least in part, in the slow dynamics of the interaction between the input-representing and the output-representing neurons. We conclude that 1) a population of CPG interneurons, recruited during a particular motor program, simultaneously encodes both the input that is used to elicit the motor program and the output elicited by this input; and 2) activity of the input-representing neurons may serve to bias the future motor programs.

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.

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.

Glutamatergic N2v Cells Are Central Pattern Generator Interneurons of the Lymnaea Feeding System: New Model for Rhythm Generation

1997 ◽  
Vol 78 (6) ◽  
pp. 3396-3407 ◽  
Author(s):  
M. J. Brierley ◽  
M. S. Yeoman ◽  
P. R. Benjamin
Keyword(s):  
Central Pattern Generator ◽  
Synaptic Connection ◽  
Giant Cells ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Rhythm Generation ◽  
Feeding System ◽  
New Model ◽  
Feeding Cycle ◽  
Protraction Phase

Brierley, M. J., M. S. Yeoman, and P. R. Benjamin. Glutamatergic N2v cells are central pattern generator interneurons of the Lymnaea feeding system: new model for rhythm generation. J. Neurophysiol. 78: 3396–3407, 1997. We aimed to show that the paired N2v (N2 ventral) plateauing cells of the buccal ganglia are important central pattern generator (CPG) interneurons of the Lymnaea feeding system. N2v plateauing is phase-locked to the rest of the CPG network in a slow oscillator (SO)-driven fictive feeding rhythm. The phase of the rhythm is reset by artificially evoked N2v bursts, a characteristic of CPG neurons. N2v cells have extensive input and output synaptic connections with the rest of the CPG network and the modulatory SO cell and cerebral giant cells (CGCs). Synaptic input from the protraction phase interneurons N1M (excitatory), N1L (inhibitory), and SO (inhibitory-excitatory) are likely to contribute to a ramp-shaped prepotential that triggers the N2v plateau. The prepotential has a highly complex waveform due to progressive changes in the amplitude of the component synaptic potentials. Most significant is the facilitation of the excitatory component of the SO → N2v monosynaptic connection. None of the other CPG interneurons has the appropriate input synaptic connections to terminate the N2v plateaus. The modulatory function of acetylcholine (ACh), the transmitter of the SO and N1M/N1Ls, was examined. Focal application of ACh (50-ms pulses) onto the N2v cells reproduced the SO → N2v biphasic synaptic response but also induced long-term plateauing (20–60 s). N2d cells show no endogenous ability to plateau, but this can be induced by focal applications of ACh. The N2v cells inhibit the N3 tonic (N3t) but not the N3 phasic (N3p) CPG interneurons. The N2v → N3t inhibitory synaptic connection is important in timing N3t activity. The N3t cells recover from this inhibition and fire during the swallow phase of the feeding pattern. Feedback N2v inhibition to the SO, N1L protraction phase interneurons prevents them firing during the retraction phase of the feeding cycle. The N2v → N1M synaptic connection was weak and only found in 50% of preparations. A weak N2v → CGC inhibitory connection prevents the CGCs firing during the rasp (N2) phase of the feeding cycle. These data allowed a new model for the Lymnaea feeding CPG to be proposed. This emphasizes that each of the six types of CPG interneuron has a unique set of synaptic connections, all of which contribute to the generation of a full CPG pattern.

A Newly Identified Buccal Interneuron Initiates and Modulates Feeding Motor Programs in Aplysia

2003 ◽  
Vol 90 (4) ◽  
pp. 2190-2204 ◽  
Author(s):  
N. C. Dembrow ◽  
J. Jing ◽  
A. Proekt ◽  
A. Romero ◽  
F. S. Vilim ◽  
...  
Keyword(s):  
Central Pattern Generator ◽  
Pattern Generator ◽  
Considerable Progress ◽  
Buccal Ganglion ◽  
Motor Programs ◽  
Cerebral Ganglia ◽  
Full Complement ◽  
Electrophysiological Characterization

Despite considerable progress in characterizing the feeding central pattern generator (CPG) in Aplysia, the full complement of neurons that generate feeding motor programs has not yet been identified. The distribution of neuropeptide-containing neurons in the buccal and cerebral ganglia can be used as a tool to identify additional elements of the feeding circuitry by providing distinctions between otherwise morphologically indistinct neurons. For example, our recent study revealed a unique and potentially interesting unpaired PRQFVamide (PRQFVa)-containing neuron in the buccal ganglion. In this study, we describe the morphological and electrophysiological characterization of this novel neuron, which we designate as B50. We found that activation of B50 is capable of producing organized rhythmic output of the feeding CPG. The motor programs elicited by B50 exhibit some similarities as well as differences to motor programs elicited by the command-like cerebral-to-buccal interneuron CBI-2. In addition to activating the feeding CPG, B50 may act as a program modulator.

scholarly journals Repetition priming of motor activity mediated by a central pattern generator: the importance of extrinsic vs. intrinsic program initiators

2016 ◽  
Vol 116 (4) ◽  
pp. 1821-1830 ◽  
Author(s):  
Michael J. Siniscalchi ◽  
Elizabeth C. Cropper ◽  
Jian Jing ◽  
Klaudiusz R. Weiss
Keyword(s):  
Motor Activity ◽  
Central Pattern Generator ◽  
Repetition Priming ◽  
Second Messengers ◽  
Pattern Generator ◽  
Motor Programs ◽  
Chemical Coding ◽  
The Core ◽  
Mediating Mechanisms ◽  
Intrinsic Program

Repetition priming is characterized by increased performance as a behavior is repeated. Although this phenomenon is ubiquitous, mediating mechanisms are poorly understood. We address this issue in a model system, the feeding network of Aplysia. This network generates both ingestive and egestive motor programs. Previous data suggest a chemical coding model: ingestive and egestive inputs to the feeding central pattern generator (CPG) release different modulators, which act via different second messengers to prime motor activity in different ways. The ingestive input to the CPG (neuron CBI-2) releases the peptides feeding circuit activating peptide and cerebral peptide 2, which produce an ingestive pattern of activity. The egestive input to the CPG (the esophageal nerve) releases the peptide small cardioactive peptide. This model is based on research that focused on a single aspect of motor control (radula opening). Here we ask whether repetition priming is observed if activity is triggered with a neuron within the core CPG itself and demonstrate that it is not. Moreover, previous studies demonstrated that effects of modulatory neurotransmitters that induce repetition priming persist. This suggests that it should be possible to “prime” motor programs triggered from within the CPG by first stimulating extrinsic modulatory inputs. We demonstrate that programs triggered after ingestive input activation are ingestive and programs triggered after egestive input activation are egestive. We ask where this priming occurs and demonstrate modifications within the CPG itself. This arrangement is likely to have important consequences for “task” switching, i.e., the cessation of one type of motor activity and the initiation of another.

The Swimming Circuit in the Pteropod Mollusk Clione limacina

2017 ◽  
pp. 569-574
Author(s):  
Yuri I. Arshavsky ◽  
Tatiana G. Deliagina ◽  
Grigory N. Orlovsky
Keyword(s):  
Nervous System ◽  
Central Pattern Generator ◽  
Rhythmic Activity ◽  
Pattern Generator ◽  
Neuronal Circuit ◽  
Basic Pattern ◽  
Marine Mollusk ◽  
Clione Limacina ◽  
Two Phases

The pelagic marine mollusk Clione limacina (class Gastropoda, subclass Opisthobranchaea, order Pteropoda), 3–5 cm in length, swims by rhythmically moving (1–2-Hz) two winglike appendages. Each swim cycle consists of two phases—the dorsal (D) and ventral (V) wing flexions. The nervous system of Clione consists of five pairs of ganglia. The wing movements are controlled by the pedal ganglia giving rise to the wing nerves. The neuronal circuit of the swim central pattern generator (CPG) is located in the pedal ganglia, which is able to generate the basic pattern of rhythmic activity after isolation from the organism (fictive swimming). Approximately 120 pedal neurons exhibit rhythmic activity during fictive swimming. According to their morphology, rhythmic neurons are divided into motoneurons (MNs), with axons exiting via the wing nerves to wing muscles, and interneurons (INs), with axons projecting to the contralateral ganglion.

Multiple mechanisms for peripheral activation of the peptide-containing radula mechanoafferent neurons B21 and B22 of Aplysia

1996 ◽  
Vol 76 (2) ◽  
pp. 1344-1351 ◽  
Author(s):  
E. C. Cropper ◽  
C. G. Evans ◽  
S. C. Rosen
Keyword(s):  
Central Pattern Generator ◽  
Sensory Neurons ◽  
Sensory Input ◽  
Pattern Generator ◽  
Contractile Properties ◽  
Mechanical Stimuli ◽  
Buccal Ganglion ◽  
Motor Programs ◽  
Peripheral Activation ◽  
Stimulation Of

1. Recently a cluster of sensory neurons (peptidergic radula mechanoafferents) has been identified in the buccal ganglion of Aplysia that is likely to play an important role in influencing the activity of feeding motor programs. All of the neurons of this cluster, which includes the identified cells B21 and B22, send axons via the radula nerve to a layer of tissue that lies under the chitinous radula (the subradula tissue). 2. We show that the subradula tissue has contractile properties. In the absence of the CNS, contractions of the subradula tissue are elicited if the subradula tissue is stretched. Alternatively, contractions are elicited when extracellular suction electrodes are used to stimulate buccal nerve 3 or the radula nerve. 3. Previous studies have shown that neurons of the B21/B22 cluster respond to peripherally applied mechanical stimuli. We show that these neurons are also activated when the subradula tissue contracts. Axon spikes (A spikes) can be intracellularly recorded from radula mechanoafferent neurons when contractions of the subradula tissue are elicited either by stretch or by extracellular stimulation of buccal nerve 3. 4. Mechanical stimuli that are subthreshold when applied alone elicit A spikes if they are applied while the subradula tissue is contracting. We postulate that this type of interaction may play an important role in gating sensory input to the feeding central pattern generator.

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