Nonlinear systems analysis of repetitive firing behavior in the crayfish stretch receptor.
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Biomedical subjects
Publications and source records attributed to D K Hartline.
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Many of the motor neurons in the lobster (Panulirus interruptus) stomatogastric ganglion exhibit plateau potentials; that is, prolonged regenerative depolarizations resulting from active membrane properties, that drive the neurons to fire impulses during bursts. Plateaus are latent in isolated ganglia but are unmasked by central input. These findings emphasize the role of cellular properties as compared to synaptic wiring in the production of cyclic motor patterns by ensembles of neurons.
1. Extra spikes may be interleaved in the otherwise rhythmic discharge pattern of the lobster stretch receptor neuron, about 2 ms after an expected spike. A constant input to the neuron is maintained by injecting current intrasomatically. The axon recovers its excitability while the retrograde invasion of the soma and dendrites is still in progress, which provide electrotonic currents to reexcite the axon. 2. While extra spikes in the axon often arise from a prolonged somatic (dendritic?) depolarization, they may also arise from a delayed retrograde invasion of the soma. 3. Failure of retrograde invasion may cause a sudden jump in the rate of rhythmic discharge, demonstrating the role of the soma-dendritic afterhyperpolarization in the regulation of rhythmic firing rate. 4. The history of repetitive firing is often important. Because extra spikes often first appear during a decline in firing rate, turning on and then off, an additional current may sometimes activate the extra spike mode, thus doubling the resting firing rate in a metastable manner. Another mestastable state is associated with failure of retrograde invasion. 5. Extra spikes augment the high end of the frequency-current curve in some receptor neurons; in other cases, the extra spikes are seen only at low rhythmic firing rates, dropping out as current reaches intermediate values to create a paradoxical negative-sensitivity region (decline in total spikes per second with increasing current). 6. The results suggest that both the extent and the speed of active retrograde invasion of the soma and dendrites are likely candidates for pathophysiological mechanisms, since they may control whether extra spikes are generated.
A comparison was made of responses of a repetitively firing neuron to perturbations imposed in an ongoing steady firing pattern with those predicted by a model termed the 'active pacemaker model' and by a simpler 'integrate-and-fire' model. The active pacemaker model simulates the kinetics of processes such as active response generation and electrogenic sodium pumping which govern the membrane potential trajectory between a reset-point following an impulse and threshold for the next impulse. Responses of the crayfish stretch receptor neuron (MRO) and of both models were studied for both abrupt steps and square pulses of current, both hyperpolarizing and depolarizing, as a function of phase of the start of the stimulus in the normal interspike interval. Physiological results are consistent with a substantially weaker effect of a perturbation delivered earlier in the interspike interval as compared to the same one given later. The active pacemaker model successfully simulates several of the prominent results of the physiology (though by no means all), while the linear integrate-and-fire model is less successful.
We have compared experimental and model studies on the rhythmic activity of the lobster stomatogastric ganglion. Both the pyloric and gastric mill systems were simulated using a physiologically based network model. In the pyloric simulation the known synaptic connectivity of the 3 principal cell types in the pyloric rhythm was found to be sufficient to produce the correct sequence of cyclic bursting activity over a substantial range of parameter values, even though we did not simulate the known endogenous oscillatory driver potential of one of the cell types. It is not yet known whether the synaptic inhibition in the real system is in the right range to cause cyclic bursting in the absence of the driver potential, but the synaptic connectivity does appear to reinforce the cyclic pattern. Simulations were also done with alternative connectivity schemes to determine which synapses appear essential to generate the correct bursting sequence (in the absence of endogenous bursting activity). Other, more complex, systems simulated were: (1) all 5 cell groups of the pyloric system, and (2) the cells responsible for movement of the lateral teeth in the gastric mill. In both cases good qualitative agreement was achieved between model and real systems.
We have applied a technique involving multi-channel linear filtering to the problem of sorting and identifying singly unit neuronal activity in records containing several simultaneously active units. The technique is effective even when the waveforms of two or more nerve impulses are superimposed. We have applied it successfully to data involving up to 6 units, and in theory it is applicable to substantially more. Current limitations are that the waveform of the impulse from each unit must first be determined by identifying and averaging several isolated examples, and that the number of recording electrodes must approximate the number of units present.
1. Acitivity patterns arising from the thirty cells of the stomatogastric ganglion of Panulirus argus are described for both a semi-intact preparation and an isolated one. 2. The thirty or so cells can be divided so far into two functional groupings: the gastric mill group, with at least ten motor elements, and the pyloric group with at least fourteen. There is some, but not extensive, interaction between groups. 3. The main gastric mill activity is arranged in two sets of elements, each of which is composed of reciprocating elements innervating antagonistic muscles. Thus alternation in activity between the single LC and the two LG neurones results in alternate closing and opening of the lateral teeth; alternation between the four GM and single CP units results in alternate protraction and retraction of the medial tooth. 4. The two sets are phased to each other in such a way that they cause gastric mill teeth to operate effectively to masticate food. 5. The main pyloric activity is arranged in a three-part cycle with each of three sets of units active in sequence. Activity in two PD and one AB unit is followed by bursts in IC and LP units followed in turn by activity in up to seven PY units. Activity in a single VD neurone is locked to this cycle in a more complex pattern.
The spontaneous burst discharges of isolated lobster (Homarus americanus) cardiac ganglia were recorded with a spaced array of electrodes. Small regions (less than 1 mm) of the ganglion were exposed to the cardioexcitor neurohormone in extracts of pericardial organs (XPO) or to 10(-5) M 5-hydroxytryptamine (5HT). All axons were excited (increased mean firing frequency, f) by both substances, but only by applications in the region between the soma (but excluding it) and proximal site of impulse initiation. Units not so exposed changed their f relatively little despite f increases of as much as threefold in exposed units and changes in burst rate and overall length. Regularity and grouping of all impulse activity into bursts was never disturbed. 5HT increases burst rate at any point of application. The increases are larger if small cells are affected than if only large cells are exposed. Burst length decreases except when the pacemaker is affected. In contrast, XPO affects neither burst rate or length unless small cells are affected. Length is increased if non-pacemaker small cells are affected; both rate and length increase if the pacemaker is affected. The pacemaker usually exhibits an f of intermediate value. Rate changes are not simply related to its f. A small cell can "burst" in the absence of impulses from any other cells. XPO may enhance endogenous "driver potentials," while 5HT may excite by depolarizing at limited sites.
Given the pattern of impulses impinging on a neuron, it should be possible to predict its output firing pattern if enough is known about pre- and postsynaptic properties. A quantitative reproduction of the first part of this input-output conversion is reported, namely the translation of input pattern into a sequence of postsynaptic membrane potential variations.
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