A Central Pattern Generator Producing Alternative Outputs: Phase Relations of Leech Heart Motor Neurons With Respect to Premotor Synaptic Input

2007 ◽  
Vol 98 (5) ◽  
pp. 2983-2991 ◽  
Author(s):  
Brian J. Norris ◽  
Adam L. Weaver ◽  
Angela Wenning ◽  
Paul S. García ◽  
Ronald L. Calabrese
Keyword(s):  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Coordination Mode ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Neuron Activity ◽  
Intersegmental Coordination ◽  
Asymmetric Pattern ◽  
Neuron Ensemble

The central pattern generator (CPG) for heartbeat in leeches consists of seven identified pairs of segmental heart interneurons and one unidentified pair. Four of the identified pairs and the unidentified pair of interneurons make inhibitory synaptic connections with segmental heart motor neurons. The CPG produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons corresponding to a similarly asymmetric fictive motor pattern in heart motor neurons, and asymmetric constriction pattern of the two tubular hearts: synchronous and peristaltic. Using extracellular techniques, we recorded, in 61 isolated nerve cords, the activity of motor neurons in conjunction with the phase reference premotor heart interneuron, HN(4), and another premotor interneuron that allowed us to assess the coordination mode. These data were then coupled with a previous description of the temporal pattern of premotor interneuron activity in the two coordination modes to synthesize a global phase diagram for the known elements of the CPG and the entire motor neuron ensemble. These average data reveal the stereotypical side-to-side asymmetric patterns of intersegmental coordination among the motor neurons and show how this pattern meshes with the activity pattern of premotor interneurons. Analysis of animal-to-animal variability in this coordination indicates that the intersegmental phase progression of motor neuron activity in the midbody in the peristaltic coordination mode is the most stereotypical feature of the fictive motor pattern. Bilateral recordings from motor neurons corroborate the main features of the asymmetric motor pattern.

Plasticity in the multifunctional buccal central pattern generator of Helisoma illuminated by the identification of phase 3 interneurons

1996 ◽  
Vol 75 (2) ◽  
pp. 561-574 ◽  
Author(s):  
E. M. Quinlan ◽  
A. D. Murphy
Keyword(s):  
Motor Activity ◽  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Neuron Activity ◽  
Phase 2 ◽  
Phase 3 ◽  
Standard Pattern

1. The mechanism for generating diverse patterns of buccal motor neuron activity was explored in the multifunctional central pattern generator (CPG) of Helisoma. The standard pattern of motor neuron activity, which results in typical feeding behavior, consists of three distinct phases of buccal motor neuron activity. We have previously identified CPG interneurons that control the motor neuron activity during phases 1 and 2 of the standard pattern. Here we identify a pair of interneurons responsible for buccal motor neuron activity during phase 3, and examine the variability in the interactions between this third subunit and other subunits of the CPG. 2. During the production of the standard pattern, phase 3 excitation in many buccal motor neurons follows a prominent phase 2 inhibitory postsynaptic potential. Therefore phase 3 excitation was previously attributed to postinhibitory rebound (PIR) in these motor neurons. Two classes of observations indicated that PIR was insufficient to account for phase 3 activity, necessitating phase 3 interneurons. 1) A subset of identified buccal neurons is inhibited during phase 3 by discrete synaptic input. 2) Other identified buccal neurons display discrete excitation during both phases 2 and 3. 3. A bilaterally symmetrical pair of CPG interneurons, named N3a, was identified and characterized as the source of phase 3 postsynaptic potentials in motor neurons. During phase 3 of the standard motor pattern, interneuron N3a generated bursts of action potentials. Stimulation of N3a, in quiescent preparations, evoked a depolarization in motor neurons that are excited during phase 3 and a hyperpolarization in motor neurons that are inhibited during phase 3. Hyperpolarization of N3a during patterned motor activity eliminated both phase 3 excitation and inhibition. Physiological and morphological characterization of interneuron N3a is provided to invite comparisons with possible homologues in other gastropod feeding CPGs. 4. These data support a model proposed for the organization of the tripartite buccal CPG. According to the model, each of the three phases of buccal motor neuron activity is controlled by discrete subsets of pattern-generating interneurons called subunit 1 (S1), subunit 2 (S2), and subunit 3 (S3). The standard pattern of buccal motor neuron activity underlying feeding is mediated by an S1-S2-S3 sequence of CPG subunit activity. However, a number of "nonstandard" patterns of buccal motor activity were observed. In particular, S2 and S3 activity can occur independently or be linked sequentially in rhythmic patterns other than the standard feeding pattern. Simultaneous recordings of S3 interneuron N3a with effector neurons indicated that N3a can account for phase-3-like postsynaptic potentials (PSPs) in nonstandard patterns. The variety of patterns of buccal motor neuron activity indicates that each CPG subunit can be active in the absence of, or in concert with, activity in any other subunit. 5. To explore how CPG activity may be regulated to generate a particular motor pattern from the CPG's full repertoire, we applied the neuromodulator serotonin. Serotonin initiated and sustained the production of an S2-S3 pattern of activity, in part by enhancing PIR in S3 interneuron N3a after the termination of phase 2 inhibition.

A Central Pattern Generator Producing Alternative Outputs: Pattern, Strength, and Dynamics of Premotor Synaptic Input to Leech Heart Motor Neurons

2007 ◽  
Vol 98 (5) ◽  
pp. 2992-3005 ◽  
Author(s):  
Brian J. Norris ◽  
Adam L. Weaver ◽  
Angela Wenning ◽  
Paul S. García ◽  
Ronald L. Calabrese
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Temporal Pattern ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Synaptic Connectivity ◽  
Neuron Activity ◽  
Coordination Modes ◽  
Asymmetric Pattern ◽  
Medicinal Leeches

The central pattern generator (CPG) for heartbeat in medicinal leeches consists of seven identified pairs of segmental heart interneurons and one unidentified pair. Four of the identified pairs and the unidentified pair of interneurons make inhibitory synaptic connections with segmental heart motor neurons. The CPG produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons corresponding to a similarly asymmetric fictive motor pattern in heart motor neurons, and asymmetric constriction pattern of the two tubular hearts, synchronous and peristaltic. Using extracellular recordings from premotor interneurons and voltage-clamp recordings of ipsilateral segmental motor neurons in 69 isolated nerve cords, we assessed the strength and dynamics of premotor inhibitory synaptic output onto the entire ensemble of heart motor neurons and the associated conduction delays in both coordination modes. We conclude that premotor interneurons establish a stereotypical pattern of intersegmental synaptic connectivity, strengths, and dynamics that is invariant across coordination modes, despite wide variations among preparations. These data coupled with a previous description of the temporal pattern of premotor interneuron activity and relative phasing of motor neuron activity in the two coordination modes enable a direct assessment of how premotor interneurons through their temporal pattern of activity and their spatial pattern of synaptic connectivity, strengths, and dynamics coordinate segmental motor neurons into a functional pattern of activity.

scholarly journals Feedback From Peripheral Musculature to Central Pattern Generator in the Neurogenic Heart of the Crab Callinectes sapidus: Role of Mechanosensitive Dendrites

2010 ◽  
Vol 103 (1) ◽  
pp. 83-96 ◽  
Author(s):  
Keyla García-Crescioni ◽  
Timothy J. Fort ◽  
Estee Stern ◽  
Vladimir Brezina ◽  
Mark W. Miller
Keyword(s):  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Callinectes Sapidus ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Neuron Spike ◽  
Effector System ◽  
Spike Bursts

The neurogenic heart of decapod crustaceans is a very simple, self-contained, model central pattern generator (CPG)-effector system. The CPG, the nine-neuron cardiac ganglion (CG), is embedded in the myocardium itself; it generates bursts of spikes that are transmitted by the CG's five motor neurons to the periphery of the system, the myocardium, to produce its contractions. Considerable evidence suggests that a CPG-peripheral loop is completed by a return feedback pathway through which the contractions modify, in turn, the CG motor pattern. One likely pathway is provided by dendrites, presumably mechanosensitive, that the CG neurons project into the adjacent myocardial muscle. Here we have tested the role of this pathway in the heart of the blue crab, Callinectes sapidus . We performed “de-efferentation” experiments in which we cut the motor neuron axons to the myocardium and “de-afferentation” experiments in which we cut or ligated the dendrites. In the isolated CG, these manipulations had no effect on the CG motor pattern. When the CG remained embedded in the myocardium, however, these manipulations, interrupting either the efferent or afferent limb of the CPG-peripheral loop, decreased contraction amplitude, increased the frequency of the CG motor neuron spike bursts, and decreased the number of spikes per burst and burst duration. Finally, passive stretches of the myocardium likewise modulated the spike bursts, an effect that disappeared when the dendrites were cut. We conclude that feedback through the dendrites indeed operates in this system and suggest that it completes a loop through which the system self-regulates its activity.

A Central Pattern Generator Producing Alternative Outputs: Temporal Pattern of Premotor Activity

2006 ◽  
Vol 96 (1) ◽  
pp. 309-326 ◽  
Author(s):  
Brian J. Norris ◽  
Adam L. Weaver ◽  
Lee G. Morris ◽  
Angela Wenning ◽  
Paul A. García ◽  
...  
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Coordination Mode ◽  
Motor Pattern ◽  
Quantitative Description ◽  
Extracellular Recording ◽  
Pattern Generator ◽  
Regular Feature ◽  
Phase Constancy ◽  
Activity State

The central pattern generator for heartbeat in medicinal leeches constitutes seven identified pairs of segmental heart interneurons. Four identified pairs of heart interneurons make a staggered pattern of inhibitory synaptic connections with segmental heart motor neurons. Using extracellular recording from multiple interneurons in the network in 56 isolated nerve cords, we show that this pattern generator produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons. This pattern corresponds to a similarly asymmetric fictive motor pattern in heart motor neurons and asymmetric constriction pattern of the two tubular hearts, synchronous and peristaltic. We provide a quantitative description of the firing pattern of all the premotor interneurons, including phase, duty cycle, and intraburst frequency of this premotor activity pattern. This analysis identifies two stereotypical coordination modes corresponding to synchronous and peristaltic, which show phase constancy over a broad range of periods as do the fictive motor pattern and the heart constriction pattern. Coordination mode is controlled through one segmental pair of heart interneurons (switch interneurons). Side-to-side switches in coordination mode are a regular feature of this pattern generator and occur with changes in activity state of these switch interneurons. Associated with synchronous coordination of premotor interneurons, the ipsilateral switch interneuron is in an active state, during which it produces rhythmic bursts, whereas associated with peristaltic coordination, the ipsilateral switch interneuron is largely silent. We argue that timing and pattern elaboration are separate functions produced by overlapping subnetworks in the heartbeat central pattern generator.

scholarly journals Output variability across animals and levels in a motor system

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Angela Wenning ◽  
Brian J Norris ◽  
Cengiz Günay ◽  
Daniel Kueh ◽  
Ronald L Calabrese
Keyword(s):  
Life History ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Motor System ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Phase Relations ◽  
The Other ◽  
Output Variability ◽  
Rhythmic Behaviors

Rhythmic behaviors vary across individuals. We investigated the sources of this output variability across a motor system, from the central pattern generator (CPG) to the motor plant. In the bilaterally symmetric leech heartbeat system, the CPG orchestrates two coordinations in the bilateral hearts with different intersegmental phase relations (Δϕ) and periodic side-to-side switches. Population variability is large. We show that the system is precise within a coordination, that differences in repetitions of a coordination contribute little to population output variability, but that differences between bilaterally homologous cells may contribute to some of this variability. Nevertheless, much output variability is likely associated with genetic and life history differences among individuals. Variability of Δϕ were coordination-specific: similar at all levels in one, but significantly lower for the motor pattern than the CPG pattern in the other. Mechanisms that transform CPG output to motor neurons may limit output variability in the motor pattern.

scholarly journals Using a Model to Assess the Role of the Spatiotemporal Pattern of Inhibitory Input and Intrasegmental Electrical Coupling in the Intersegmental and Side-to-Side Coordination of Motor Neurons by the Leech Heartbeat Central Pattern Generator

2008 ◽  
Vol 100 (3) ◽  
pp. 1354-1371 ◽  
Author(s):  
Paul S. García ◽  
Terrence M. Wright ◽  
Ian R. Cunningham ◽  
Ronald L. Calabrese
Keyword(s):  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Electrical Coupling ◽  
Pattern Generator ◽  
Living System ◽  
Phase Relations ◽  
Spatiotemporal Pattern ◽  
Intrinsic Properties ◽  
Synaptic Inputs

Previously we presented a quantitative description of the spatiotemporal pattern of inhibitory synaptic input from the heartbeat central pattern generator (CPG) to segmental motor neurons that drive heartbeat in the medicinal leech and the resultant coordination of CPG interneurons and motor neurons. To begin elucidating the mechanisms of coordination, we explore intersegmental and side-to-side coordination in an ensemble model of all heart motor neurons and their known synaptic inputs and electrical coupling. Model motor neuron intrinsic properties were kept simple, enabling us to determine the extent to which input and electrical coupling acting together can account for observed coordination in the living system in the absence of a substantive contribution from the motor neurons themselves. The living system produces an asymmetric motor pattern: motor neurons on one side fire nearly in synchrony (synchronous), whereas on the other they fire in a rear-to-front progression (peristaltic). The model reproduces the general trends of intersegmental and side-to-side phase relations among motor neurons, but the match with the living system is not quantitatively accurate. Thus realistic (experimentally determined) inputs do not produce similarly realistic output in our model, suggesting that motor neuron intrinsic properties may contribute to their coordination. By varying parameters that determine electrical coupling, conduction delays, intraburst synaptic plasticity, and motor neuron excitability, we show that the most important determinant of intersegmental and side-to-side phase relations in the model was the spatiotemporal pattern of synaptic inputs, although phasing was influenced significantly by electrical coupling.

Heartbeat Control in Leeches. II. Fictive Motor Pattern

2004 ◽  
Vol 91 (1) ◽  
pp. 397-409 ◽  
Author(s):  
Angela Wenning ◽  
Andrew A. V. Hill ◽  
Ronald L. Calabrese
Keyword(s):  
Motor Neurons ◽  
Sensory Feedback ◽  
Coordination Mode ◽  
Motor Pattern ◽  
Preceding Paper ◽  
Rhythmic Activity ◽  
Pattern Generator ◽  
Inhibitory Input ◽  
Combine Data ◽  
Coordination Modes

The rhythmic beating of the tube-like hearts in the medicinal leech is driven and coordinated by rhythmic activity in segmental heart motor neurons. The motor neurons are controlled by rhythmic inhibitory input from a network of heart interneurons that compose the heartbeat central pattern generator. In the preceding paper, we described the constriction pattern of the hearts in quiescent intact animals and showed that one heart constricts in a rear-to-front wave (peristaltic coordination mode), while the other heart constricts in near unison over its length (synchronous coordination mode) and that they regularly switch coordination modes. Here we analyze intersegmental and side-to-side-coordination of the fictive motor pattern for heartbeat in denervated nerve cords. We show that the intersegmental phase relations among heart motor neurons in both coordination modes are independent of heartbeat period. This finding enables us to combine data from different experiments to form a detailed analysis of the relative phases, duty cycle, and intraburst spike frequency of the bursts of the segmental heart motor neurons. The fictive motor pattern and the constriction pattern seen in intact leeches closely match in their intersegmental and side-to-side coordination, indicating that sensory feedback is not necessary for properly phased intersegmental coordination. Moreover, the regular switches in coordination mode of the fictive motor pattern mimic those seen in intact animals indicating that these switches likely arise by a central mechanism.

Neurotransmitter Interactions in the Stomatogastric System of the Spiny Lobster: One Peptide Alters the Response of a Central Pattern Generator to a Second Peptide

1997 ◽  
Vol 77 (2) ◽  
pp. 599-610 ◽  
Author(s):  
Patsy S. Dickinson ◽  
Wesley P. Fairfield ◽  
John R. Hetling ◽  
Jane Hauptman
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Spiny Lobster ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Stomatogastric Nervous System ◽  
Panulirus Interruptus ◽  
State Dependent ◽  
Bursting Activity ◽  
Stomatogastric System

Dickinson, Patsy S., Wesley P. Fairfield, John R. Hetling, and Jane Hauptman. Neurotransmitter interactions in the stomatogastric system of the spiny lobster: one peptide alters the response of a central pattern generator to a second peptide. J. Neurophysiol. 77: 599–610, 1997. Two of the peptides found in the stomatogastric nervous system of the spiny lobster, Panulirus interruptus, interacted to modulate the activity of the cardiac sac motor pattern. In the isolated stomatogastric ganglion, red-pigment-concentrating hormone (RPCH), but not proctolin, activated the bursting activity in the inferior ventricular (IV) neurons that drives the cardiac sac pattern. The cardiac sac pattern normally ceased within 15 min after the end of RPCH superfusion. However, when proctolin was applied within a few minutes of that time, it was likewise able to induce cardiac sac activity. Similarly, proctolin applied together with subthreshold RPCH induced cardiac sac bursting. The amplitude of the excitatory postsynaptic potentials from the IV neurons to the cardiac sac dilator neuron CD2 (1 of the 2 major motor neurons in the cardiac sac system) was potentiated in the presence of both proctolin and RPCH. The potentiation in RPCH was much greater than in proctolin alone. However, the potentiation inproctolin after RPCH was equivalent to that recorded in RPCH alone. Although we do not yet understand the mechanisms for these interactions of the two modulators, this study provides an example of one factor that can determine the “state” of the system that is critical in determining the effect of a modulator that is “state dependent,” and it provides evidence for yet another level of flexibility in the motor output of this system.

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

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

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

Aplysia ink release: central locus for selective sensitivity to long-duration stimuli

1979 ◽  
Vol 42 (5) ◽  
pp. 1223-1232 ◽  
Author(s):  
E. Shapiro ◽  
J. Koester ◽  
J. H. Byrne
Keyword(s):  
Motor Neuron ◽  
Spike Train ◽  
Motor Neurons ◽  
Neural Circuit ◽  
Reversal Potential ◽  
Secretory Process ◽  
Neuron Activity ◽  
Long Duration ◽  
Noxious Stimuli ◽  
Selective Sensitivity

1. A behavioral and electrophysiological analysis of defensive ink release in Aplysia californica was performed to examine the response of this behavior and its underlying neural circuit to various-duration noxious stimuli. 2. Three separate behavioral protocols were employed using electrical shocks to the head as noxious stimuli to elicit ink release. Ink release was found to be selectively responsive to longer duration stimuli, and to increase in a steeply graded fashion as duration is increased. 3. Intracellular stimulation of ink motor neurons revealed that ink release is a linear function of motor neuron spike train duration, indicating that the selective sensitivity of the behavior to long-duration stimuli is not due to a nonlinearity in the glandular secretory process. 4. In contrast, electrophysiological examination of ink motor neuron activity in response to sustained head shock revealed an accelerating spike train. During the later part of the spike train, compound excitatory synaptic potentials show a positive shift in reversal potential. 5. Our results suggest a central locus for the mechanisms that determine sensitivity of inking behavior to stimulus duration. 6. In contrast to ink release, defensive gill withdrawal was found to be extremely sensitive to short-duration stimuli.

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