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 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.

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.

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.

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.

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.

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.

Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61

1986 ◽  
Vol 122 (1) ◽  
pp. 277-302
Author(s):  
M. P. Nusbaum ◽  
W. B. Kristan
Keyword(s):  
Central Pattern Generator ◽  
Motor Pattern ◽  
Pattern Generator ◽  
The Other ◽  
Sensory Neurones ◽  
Segmental Nerve ◽  
Macrobdella Decora ◽  
Intracellular Stimulation ◽  
Retzius Cell ◽  
Stimulation Of

Two pairs of serotonin-containing neurones, designated cells 21 and 61, were characterized physiologically and anatomically in the hirudinid leeches Macrobdella decora and Hirudo medicinalis. Both of these cells are bilaterally paired interneurones and each cell is weakly electrically coupled to the other serotonin-containing cells both intra- and interganglionically. Cells 21 and 61 are excited polysynaptically by individual identified mechano-sensory neurones. Segmental nerve shock sufficient to elicit an episode of swimming strongly excites cells 21 and 61, which then tend to generate bursts of impulses that are phase-locked to the swim motor pattern. Intracellular stimulation of either cell 21 or cell 61 often causes the initiation of swimming, acting in parallel with the nonserotonergic swim-initiator cell 204. Cells 61 and 204 are also weakly electrically coupled. The latency to swim onset by stimulating cell 21 or 61 is similar to that of cell 204 and different from that of the serotonergic Retzius cell. This result, with those in the accompanying paper (Nusbaum, 1986), suggests that unlike the Retzius cell and similar to cell 204, cells 21 and 61 synaptically contact cells of the swim central pattern generator (CPG).

Gating of Afferent Input by a Central Pattern Generator

1999 ◽  
Vol 81 (2) ◽  
pp. 950-953 ◽  
Author(s):  
Ralph A. DiCaprio
Keyword(s):  
Central Pattern Generator ◽  
Sensory Input ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Afferent Input ◽  
Inhibitory Input ◽  
Cycle Period ◽  
Intracellular Recordings ◽  
Afferent Fibers ◽  
Sufficient Magnitude

Gating of afferent input by a central pattern generator. Intracellular recordings from the sole proprioceptor (the oval organ) in the crab ventilatory system show that the nonspiking afferent fibers from this organ receive a cyclic hyperpolarizing inhibition in phase with the ventilatory motor pattern. Although depolarizing and hyperpolarizing current pulses injected into a single afferent will reset the ventilatory motor pattern, the inhibitory input is of sufficient magnitude to block afferent input to the ventilatory central pattern generator (CPG) for ∼50% of the cycle period. It is proposed that this inhibitory input serves to gate sensory input to the ventilatory CPG to provide an unambiguous input to the ventilatory CPG.

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.

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