Initiation, Maintenance and Modulation of Swimming in the Medicinal Leech by the Activity of a Single Neurone

1978 ◽  
Vol 77 (1) ◽  
pp. 71-88 ◽  
Author(s):  
JAMS C. WEEKS ◽  
WILLIAM B. KRISTAN JR.

A neurone (designated cell 204) has been identified in the segmental ganglia of the leech which, when stimulated intracellularly in isolated nerve cords, reliably initiates and maintains the neuronal activity pattern characteristic of swimming. In a minimally dissected leech, cell 204 activity results in normal swimming movements. Cell 204 is an unpaired, intersegmental interneurone which is present in most, if not all, of the segmental ganglia. Horseradish peroxidase injections indicate that cell 204 has extensive arborizations in its own ganglion and sends an axon both anteriorly and posteriorly via Faivre's Nerve. Cell 204 is normally quiescent, but during swimming activity becomes depolarized and produces impulse bursts in the ventral contraction phase of its own segment. Such activity is observed in every cell 204 in the nerve cord and is independent of the stimulus used to evoke the swimming episode. Activity in any cell 204 is sufficient for initiation and maintenance of swimming activity, whereas activity in any two of them is not necessary for swimming. During swimming activity, imposed increases in the impulse frequency of any cell 204 cause a decrease in the swim cycle period of the entire nerve cord. Tactile stimulation of the skin, which is an effective method of eliciting swimming episodes, excites cell 204. Our findings indicate that cell 204 may activate swimming in the intact leech.

1986 ◽  
Vol 55 (5) ◽  
pp. 977-994 ◽  
Author(s):  
E. A. Debski ◽  
W. O. Friesen

Swimming activity evoked by light tactile stimulation of a body wall flap in dissected leech preparations undergoes habituation (5). In this study, we examine the activity of several interneurons (cell 204, cell 205, the S cell, and cell 208) during habituation trials to study further the neuronal mechanisms that mediate this decline in responsiveness. Light tactile stimulation of the leech body wall evoked initially a marked excitatory response in cell 204 homologs (segmental swim-initiating neurons) that preceded the initiation of swimming activity. This response decreased over the course of repeated stimulus trials; however, no marked decline in cell 204 activity accompanied the cessation of swim initiation. A similar activity pattern was observed in cell 205. Thus the habituation of swimming activity to stroking of the body wall is not due solely to reduced input to cell 204 and cell 205. The early activity of cell 204 was not correlated to the duration of subsequent swim episodes. However, the impulse frequency of cell 204 during swim episodes was negatively correlated to the period of swim cycles. This correlation between cell 204 activity and cycle period occurred both within individual episodes as well as between trials in a habituation series. Direct stimulation of cell 204 with current pulses evoked swimming activity reliably for an average of 72 trials. Therefore, habituation that results from stroking the body wall (which occurs after approximately 6 trials) is not mediated by plasticity in the connections between cell 204 and the swim oscillator. The S cell fired repeatedly in response to light tactile stimulation. This response declined with repeated trials. Intense intracellular stimulation of the S cell was sufficient to initiate swimming activity in some preparations. The magnitude and duration of the excitation required to initiate swimming by this means were far greater, however, than that which occurred during stroking the body wall. The response of cell 208 (a swim oscillator cell) to body wall stimulation during habituation trials was variable; usually an initial hyperpolarization was followed by some depolarization. No aspect of this response correlated with the onset of habituation. Our results are consistent with the idea that cell 204 and cell 205 are part of the pathway that mediates swimming activity in response to light tactile stimulation of the leech body wall, and that habituation occurs, in part, as the result of reduced sensory input to this cell.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 116 (1) ◽  
pp. 169-188
Author(s):  
E. A. Debski ◽  
W. O. Friesen

Tactile stimulation (light stroking) of a body wall flap attached to the ventral nerve cord of the medicinal leech evokes episodes of swimming activity. This swimming response undergoes habituation, involving changes in swim initiation and swim maintenance. Repeated stimulation of the body wall flap evoked swimming activity between three and 39 times before this response failed. During repetitive stimulation, the length of swim episodes decreased by about 50%. The number of swim episodes which could be elicited was not correlated with swim episode length. Following habituation, swim initiation showed significant spontaneous recovery, but swim episode length returned only to 60% of control values. In preparations where spontaneous recovery was followed by rehabituation, the number of swim episodes elicited declined with each habituation-recovery sequence. Additional stimulation immediately following habituation trials had a dual effect: recovery of the swimming response was delayed, but the lengths of swim episodes following spontaneous recovery were increased. Pinching the body wall flap immediately restored the swimming response in an habituated preparation. Swim initiation habituated more rapidly during stimulation of anterior body wall flaps than during stimulation of mid-body or posterior flaps. However, swim length was independent of this regional variation in swim responsiveness. The number of swim episodes elicited by stimulation of body wall flaps attached to posterior or anterior segments depended upon whether this segment was stimulated before or after other flaps. In contrast, in mid-body segments there was no evidence for such stimulus generalization. The lengths of swim episodes elicited during sequential stimulation of several body wall flaps were independent of the stimulation sequence. We propose that separate processes control swim initiation and swim maintenance. These processes must be repeated in most, if not all, of the segmental ganglia of the leech ventral nerve cord.


1973 ◽  
Vol 59 (3) ◽  
pp. 675-696
Author(s):  
R. J. COOTER

1. Visual and multimodal units were recorded from the thoracic nerve cord of the cockroach, Periplaneta americana, using glass microelectrodes. 2. Compound-eye units could be classified as ON-, OFF- or ON-OFF-units according to their response to visual stimulation. Some were multimodal, firing to both visual and tactile stimulation of the antennae. 3. Although some units were found to be either fired by ipsilateral or by contralateral stimulation only, others were fired by both types of stimulation, often in different ways. 4. Ocellar units were invariably OFF-units, mainly phasic, but one type showed tonic dark-firing in addition to the phasic OFF-burst. 5. The general properties of cockroach visual units are discussed and compared with those reported by other workers for different insects.


1985 ◽  
Vol 54 (6) ◽  
pp. 1444-1459 ◽  
Author(s):  
R. A. Pearce ◽  
W. O. Friesen

The isolated leech nervous system generates a metachronally coordinated rhythmic output that is the neuronal correlate of swimming activity. We investigated two factors that contribute to intersegmental coordination: the swim-cycle periods expressed by segmental ganglia and the strength of neuronal coupling between ganglia. To determine the regional variation in swim-cycle periods, we severed both of the lateral intersegmental connectives. We left intact the median connective, which conveys tonic excitation but little phasic information. We obtained a reduction in intersegmental coupling strength by severing a single lateral intersegmental connective. Cycle periods were manipulated by cooling restricted sections of the nerve cord. Our experiments revealed an anterior-posterior gradient of cycle periods in ganglia of the isolated nerve cord; that is, chains of ganglia obtained from the anterior nerve cord exhibited longer cycle periods than those obtained from the posterior end of the cord. This gradient extends posteriorly to approximately ganglion 12 and may reverse posterior to ganglion 13. Increasing local cycle periods by cooling restricted sections of the nerve cord caused delay in activity cycles in the cooled ganglia, relative to the cycles of ganglia at the control temperature. This finding demonstrates that the observed gradient in cycle period provides for smaller intersegmental phase lags than would occur if there were no period gradients. Reduction of coupling strength by severing a lateral connective led to altered phase relationships across the lesion, both at the motor and oscillator levels. For those ganglion chains in which the anterior ganglia had greater periods, the reduced coupling led to reduced or even reversed phase relationships across the lesion but left unchanged the phase lag between the ends of the chain. In contrast, reduced coupling between halves of a chain in which the posterior ganglia had greater cycle periods led to increased phase lags across the lesion and between the ends. These altered phase relationships arise from a relative increase in the contribution of period differences when coupling strength is decreased. We conclude that the anterior-to-posterior progression of neuronal activity in the isolated leech nerve cord during swimming activity is provided by the intersegmental coupling signals. Furthermore, the period gradient expressed in our preparations acts to provide for smaller phase lags than would be generated by these coupling signals in the absence of such a gradient.(ABSTRACT TRUNCATED AT 400 WORDS)


1978 ◽  
Vol 75 (1) ◽  
pp. 45-63
Author(s):  
M. Poon ◽  
W. O. Friesen ◽  
G. S. Stent

A network of intra- and intersegmental synaptic connexions has been identified in the ventral nerve cord of the leech that links the set of oscillatory interneurones of the central swim oscillator to the motor neurones commanding the swimming rhythm. Excitatory connexions lead from oscillatory interneurones to both excitatory and inhibitory motor neurones, whereas inhibitory connexions lead from oscillatory interneurones to only the inhibitory motor neurones. Connexions leading from a motor neurone back to the oscillatory interneurones were found in only one exceptional case, an inhibitory motor neurone previously known to have access to the central swim oscillator. This network of identified connexions can account reasonably well for the mechanism by which the oscillatory interneurones drive their follower motor neurones into the phasic activity pattern characteristic of the swimming movement.


1978 ◽  
Vol 75 (1) ◽  
pp. 25-43
Author(s):  
W. O. Friesen ◽  
M. Poon ◽  
G. S. Stent

Four oscillatory interneurones that appear to be the principal components of the central swim oscillator of Hirudo medicinalis have been identified on each side of the segmental ganglia of the ventral nerve cord. During ‘swimming’ episodes of an isolated nerve cord preparation each interneurone undergoes a polarization rhythm that is phase-locked with the impulse burst rhythm of the motor neurones known to drive the swimming movement. Passage of current into any of the interneurones can shift the phase of the swim rhythm. One of the interneurones projects its axon rearward to posterior ganglia and the other three project their axons frontward to anterior ganglia. The oscillatory interneurones are connected both intra- and interganglionically to form a topologically complex intersegmental network of concatenated ring circuits that possess the feature of recurrent cyclic inhibition. Theoretical analysis and electronic analogue models show that the network is inherently oscillatory and can produce both a cycle period and intra- and intersegmental phase relations of its elements that are appropriate for generating the body wave of the swimming movement.


1982 ◽  
Vol 47 (5) ◽  
pp. 885-908 ◽  
Author(s):  
R. Gillette ◽  
M. P. Kovac ◽  
W. J. Davis

1. A population of interneurons that control feeding behavior in the mollusk Pleurobranchaea has been analyzed by dye injection and intracellular stimulation/recording in whole animals and reduced preparations. The population consists of 12-16 somata distributed in two bilaterally symmetrical groups on the anterior edge of the cerebropleural ganglion (brain). On the basis of their position adjacent to the cerebral lobes, these cells have been named paracerebral neurons (PCNs). This study concerns pme subset pf [MCs. the large, phasic ones, which have the strongest effect on the feeding rhythm (21). 2. Each PCN sends a descending axon via the ipsilateral cerebrobuccal connective to the buccal ganglion. Axon branches have not been detected in other brain or buccal nerves and hence the PCNs appear to be interneurons. 3. In whole-animal preparations, tonic intracellular depolarization of the PNCs causes them to discharge cyclic bursts of action potentials interrupted by a characteristic hyperpolarization. In all specimens that exhibit feeding behavior, the interburst hyperpolarization is invariably accompanied by radula closure and the beginning of proboscis retraction (the "bite"). No other behavorial effect of PCN stimulation has been observed. 4. In whole-animal preparations, the PCNs are excited by food and tactile stimulation of the oral veil, rhinophores, and tentacles. When such stimuli induce feeding the PCNs discharge in the same bursting pattern seen during tonic PCN depolarization, with the cyclic interburst hyperpolarization phase locked to the bit. When specimens egest an unpalatable object by cyclic buccal movements, however, the PCNs are silent. The PCNs therefore exhibit properties expected of behaviorally specific "command" neurons for feeding. 5. Silencing one or two PCNs by hyperpolarization may weaken but does not prevent feeding induced by natural food stimuli. Single PCNs therefore can be sufficient but are not necessary to induction of feeding behavior. Instead the PCNs presumably operate as a population to control feeding. 6. In isolated nervous system preparations tonic extracellular stimulation of the stomatogastric nerve of the buccal ganglion elicits a cyclic motor rhythm that is similar in general features to the PNC-induced motor rhythm. Bursts of PCN action potentials intercalated at the normal phase position in this cycle intensify the buccal rhythm. Bursts of PCN impulses intercalated at abnormal phase positions reset the buccal rhythm. The PCNs, therefore, also exhibit properties expected of pattern-generator elements and/or coordinating neurons for the buccal rhythm. 7. The PCNs are recruited into activity when the buccal motor rhythm is elicited by stomatogastric nerve stimulation or stimulation of the reidentifiable ventral white cell. The functional synergy between the PCNs and the buccal rhythm is therefore reciprocal. 8...


1991 ◽  
Vol 260 (5) ◽  
pp. H1522-H1530 ◽  
Author(s):  
T. E. Pisarri ◽  
A. Jonzon ◽  
H. M. Coleridge ◽  
J. C. Coleridge

Intravenous injection of hypertonic NaCl solution evokes reflex bradycardia and hypotension, effects thought to result from stimulation of afferent vagal endings in the lungs. To identify the afferents responsible for these effects, we recorded vagal impulses arising from endings in the lungs and lower airways of anesthetized dogs and examined the response to injection of hypertonic solutions into the pulmonary circulation. Injection of 4,800 mmol/l NaCl solution (1 ml/kg) stimulated 39 of 49 pulmonary C-fibers, their impulse frequency increasing 35-fold. Stimulation was concentration dependent, the minimum effective concentration being between 1,200 and 4,800 mmol/l. Rapidly adapting receptors were also stimulated in a concentration-dependent manner, 35 of 41 receptors being stimulated by 4,800 mmol/l NaCl solution, firing increasing fivefold. Bronchial C-fibers were not stimulated by injection into the pulmonary circulation but were by injection into the bronchial artery. Hypertonic urea solutions had qualitatively similar but smaller effects on pulmonary C-fibers and rapidly adapting receptors. The results suggest that the reflex effects of intravenous injection of hypertonic solutions result principally from stimulation of pulmonary C-fibers.


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