scholarly journals Feedforward discharges couple the singing central pattern generator and ventilation central pattern generator in the cricket abdominal central nervous system

2019 ◽  
Vol 205 (6) ◽  
pp. 881-895 ◽  
Author(s):  
Stefan Schöneich ◽  
Berthold Hedwig

Abstract We investigated the central nervous coordination between singing motor activity and abdominal ventilatory pumping in crickets. Fictive singing, with sensory feedback removed, was elicited by eserine-microinjection into the brain, and the motor activity underlying singing and abdominal ventilation was recorded with extracellular electrodes. During singing, expiratory abdominal muscle activity is tightly phase coupled to the chirping pattern. Occasional temporary desynchronization of the two motor patterns indicate discrete central pattern generator (CPG) networks that can operate independently. Intracellular recordings revealed a sub-threshold depolarization in phase with the ventilatory cycle in a singing-CPG interneuron, and in a ventilation-CPG interneuron an excitatory input in phase with each syllable of the chirps. Inhibitory synaptic inputs coupled to the syllables of the singing motor pattern were present in another ventilatory interneuron, which is not part of the ventilation-CPG. Our recordings suggest that the two centrally generated motor patterns are coordinated by reciprocal feedforward discharges from the singing-CPG to the ventilation-CPG and vice versa. Consequently, expiratory contraction of the abdomen usually occurs in phase with the chirps and ventilation accelerates during singing due to entrainment by the faster chirp cycle.

2016 ◽  
Vol 116 (4) ◽  
pp. 1728-1742 ◽  
Author(s):  
Akira Sakurai ◽  
Paul S. Katz

The nudibranch mollusc, Dendronotus iris, swims by rhythmically flexing its body from left to right. We identified a bilaterally represented interneuron, Si3, that provides strong excitatory drive to the previously identified Si2, forming a half-center oscillator, which functions as the central pattern generator (CPG) underlying swimming. As with Si2, Si3 inhibited its contralateral counterpart and exhibited rhythmic bursts in left-right alternation during the swim motor pattern. Si3 burst almost synchronously with the contralateral Si2 and was coactive with the efferent impulse activity in the contralateral body wall nerve. Perturbation of bursting in either Si3 or Si2 by current injection halted or phase-shifted the swim motor pattern, suggesting that they are both critical CPG members. Neither Si2 nor Si3 exhibited endogenous bursting properties when activated alone; activation of all four neurons was necessary to initiate and maintain the swim motor pattern. Si3 made a strong excitatory synapse onto the contralateral Si2 to which it is also electrically coupled. When Si3 was firing tonically but not exhibiting bursting, artificial enhancement of the Si3-to-Si2 synapse using dynamic clamp caused all four neurons to burst. In contrast, negation of the Si3-to-Si2 synapse by dynamic clamp blocked ongoing swim motor patterns. Together, these results suggest that the Dendronotus swim CPG is organized as a “twisted” half-center oscillator in which each “half” is composed of two excitatory-coupled neurons from both sides of the brain, each of which inhibits its contralateral counterpart. Consisting of only four neurons, this is perhaps the simplest known network oscillator for locomotion.


1999 ◽  
Vol 81 (2) ◽  
pp. 950-953 ◽  
Author(s):  
Ralph A. DiCaprio

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.


2003 ◽  
Vol 89 (4) ◽  
pp. 2120-2136 ◽  
Author(s):  
Itay Hurwitz ◽  
Irving Kupfermann ◽  
Klaudiusz R. Weiss

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.


1995 ◽  
Vol 73 (3) ◽  
pp. 1013-1019 ◽  
Author(s):  
R. Perrins ◽  
A. Roberts

1. We have investigated whether in Xenopus embryos, spinal interneurons of the central pattern generator (CPG) receive cholinergic or electrical excitatory input during swimming. The functions of cholinergic excitation during swimming were also investigated. 2. Intracellular recordings were made from rhythmically active presumed premotor interneurons in the dorsal third of the spinal cord. After locally blocking inhibitory potentials with 2 microM strychnine and 40 microM bicuculline, the reliability of spike firing and the amplitude of fast, on-cycle, excitatory postsynaptic potentials (EPSPs) underlying the single on-cycle spikes were measured during fictive swimming. 3. The nicotinic antagonists d-tubocurarine and dihydro-beta-erythroidine (DH beta E, both 10 microM) reversibly reduced the reliability of the spike firing during swimming and reduced the amplitude of the on-cycle EPSP by 16%. DH beta E also reduced the EPSP amplitude in spinalized embryos by 22%. These results indicate that interneurons receive rhythmic cholinergic excitation from a source within the spinal cord. 4. Combined applications of nicotinic and excitatory amino acid (EAA) antagonists or cadmium (Cd2+, 100-200 microM) resulted in complete block of the fast EPSP, suggesting that interneurons do not receive electrical excitation. 5. The nicotinic antagonists mecamylamine and d-tubocurarine (both 5 microM) reduced the duration of episodes of fictive swimming recorded from the ventral roots, in spinal embryos. When applied in the middle of a long episode, d-tubocurarine decreased the swimming frequency, ruling out an effect on the initiation pathway. The cholinesterase inhibitor eserine (10 microM) increased the duration of swimming episodes.(ABSTRACT TRUNCATED AT 250 WORDS)


1982 ◽  
Vol 98 (1) ◽  
pp. 195-211
Author(s):  
ANDREW D. McCLELLAN

Feeding, regurgitation, and rejection in the marine gastropod Pleurobranchaea all involve similar but not identical rhythmic movements of buccal mass structures such as the radula, jaws and lips. The part of the motor pattern which produces rhythmic radula movement, as recorded in the major external muscles of the buccal mass of behaving semi-intact preparations, was similar during the three different types of behaviour, suggesting that they share a common motor-pattern generator. Other parts of the motor pattern were only obviously different during the vomiting phase of regurgitation. Differences in the function and motor patterns of feeding and rejection are presumably accounted for by differences in the activity of muscles which could not be recorded from in this study (e.g. jaw muscles). A general conclusion is that buccal rhythms in gastropods cannot automatically be assumed to underlie feeding, and this is particularly true for dissected preparations which do not execute a clear behavioural response. It would be necessary either to record motor activity that is unique for a given behaviour, or to employ preparations which execute unambiguous behavioural responses.


2000 ◽  
Vol 203 (22) ◽  
pp. 3505-3512 ◽  
Author(s):  
R.J. Wilson ◽  
M.B. Harris ◽  
J.E. Remmers ◽  
S.F. Perry

While little is known of the origin of air-breathing in vertebrates, primitive air breathers can be found among extant lobe-finned (Sarcopterygii) and ray-finned (Actinopterygii) fish. The descendents of Sarcopterygii, the tetrapods, generate lung ventilation using a central pattern generator, the activity of which is modulated by central and peripheral CO(2)/H(+) chemoreception. Air-breathing in Actinopterygii, in contrast, has been considered a ‘reflexive’ behaviour with little evidence for central CO(2)/H(+) respiratory chemoreceptors. Here, we describe experiments using an in vitro brainstem preparation of a primitive air-breathing actinopterygian, the longnose gar Lepisosteus osseus. Our data suggest (i) that gill and air-breathing motor patterns can be produced autonomously by the isolated brainstem, and (ii) that the frequency of the air-breathing motor pattern is increased by hypercarbia. These results are the first evidence consistent with the presence of an air-breathing central pattern generator with central CO(2)/H(+) respiratory chemosensitivity in any primitive actinopterygian fish. We speculate that the origin of the central neuronal controller for air-breathing preceded the divergence of the sarcopterygian and actinopterygian lineages and dates back to a common air-breathing ancestor.


1996 ◽  
Vol 75 (2) ◽  
pp. 561-574 ◽  
Author(s):  
E. M. Quinlan ◽  
A. D. Murphy

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.


1988 ◽  
Vol 60 (6) ◽  
pp. 2122-2137 ◽  
Author(s):  
S. N. Currie ◽  
P. S. Stein

1. A low-spinal, immobilized turtle displays a fictive scratch reflex in hindlimb motor neurons in response to tactile stimulation of the shell (17, 19). Turtles exhibit three forms of the scratch reflex: rostral, pocket, and caudal. Each form is elicited by tactile stimulation of a different receptive field on the body surface. The ventral-posterior pocket (VPP) cutaneous nerve innervates the ventral-posterior portion of the pocket scratch receptive field (Fig. 1). Natural stimulation within the VPP nerve's receptive field evoked a pocket scratch reflex (Fig. 2A). Electrical stimulation of this nerve elicited robust pocket scratch reflexes (Fig. 2, B and C). 2. A single electrical pulse to the VPP nerve delivered at a voltage (greater than 5 V, 0.1 ms) that activated all the axons in the nerve was termed a "maximal" pulse. A single maximal pulse did not evoke a scratch motor response. It raised the excitability of the pocket scratch central pattern generator for several seconds, however. We revealed such excitability changes by applying maximal pulses to the VPP nerve at multisecond intervals (Figs. 5 and 6). When we delivered maximal pulses with interpulse intervals of less than or equal to 5 s, the first pulse produced no motor response and the second pulse evoked one or more cycles of pocket scratch. 3. A stimulus pulse applied to the VPP nerve was used as a probe for studying changes in the excitability of the pocket scratch CPG following scratch motor patterns. In a rested preparation, the stimulus pulse did not activate motor output. In contrast, the stimulus pulse evoked one or two cycles of pocket scratch activity if delivered within 2.5 s after the cessation of rhythmic pocket scratch motor activity (Figs. 7-9). These results are consistent with the hypothesis that the pocket scratch CPG has elevated excitability for seconds following the cessation of pocket scratch motor output. A single pulse applied to the VPP nerve evoked no response if delivered after the cessation of rostral scratch motor activity, however (Fig. 9D). 4. We used a train of maximal pulses to the VPP nerve to probe the form-specificity of the changes in the excitability following a rostral scratch motor pattern (Fig. 10). We set the stimulus parameters so that the train evoked one or two cycles of a pocket scratch motor pattern in a preparation that had rested for over 1 min.(ABSTRACT TRUNCATED AT 400 WORDS)


1982 ◽  
Vol 99 (1) ◽  
pp. 185-196 ◽  
Author(s):  
J. A. Kahn ◽  
A. Roberts

Rhythmic motor nerve activity was recorded in stage 37/38 Xenopus embryos paralysed with curare. The activity was similar to the swimming motor pattern in the following ways: cycle period (40–125 ms), alternation of activity on either side of a segment, rostro-caudal phase lag. Episodes of rhythmic motor activity could be evoked by stimuli that evoke swimming and inhibited by stimuli that normally inhibit swimming. On this basis we conclude that the swimming motor pattern is generated by a central nervous mechanism and is not dependent on sensory feedback. In addition to the swimming pattern, another pattern of motor activity (‘synchrony’) was sometimes recorded in curarized embryos. In this, the rhythmic bursts on either side of a segment occurred in synchrony, and the rhythm period (20–50 ms) was half that in swimming. This was probably not an artifact of curarization as there were indications of a similar pattern in uncurarized embryos. Its function remains unclear.


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