Slowly adapting stretch-receptor organs: periodic stimulation with and without perturbations.
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Biomedical subjects
Publications and source records attributed to J P Segundo.
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The relation between a maintained spatial orientation and the corresponding fully adapted discharge rate was multivalued in all the afferents tonically sensitive to maintained spatial orientation observed in isolated utricles of Rhinobates productus. The spread of rate values was of the order of changes produced by natural tilts. The occurrence of multivaluedness in isolated receptors indicated that peripheral issues are sufficient. Two factors contributed: firstly, the side from which the orientation had been reached (i.e. "hysteresis"): higher adapted rates occurred when the preceding orientation was characterized by lower rates and when the corresponding transition caused acceleration; secondly, "spontaneous" rate variations, some of which resembled markedly, and interacted with, the effects of tilts. It was not possible to identify the basic mechanisms underlying these factors. The multivaluedness in the coding of maintained position, because of its constancy and magnitude, cannot be ignored. It, as well as the sensitivity to fast transients, must be taken into account in utricular models, in evaluations of information transmission, and in psychophysical explorations.
The degree of axo-axonal synaptic coupling between nerve cells in the buccal ganglion of Navanax was investigated in relation to intracellular ionic calcium. Increasing intracellular Ca2+ by injection of Ca2+, injection of Na+, or application of ionophore X537A produced uncoupling after at least 90 min, if metabolic inhibitor was present in the medium. Subsequent removal of the metabolic inhibitor reestablished the coupling in less than 30 min. Injected Sr2+ also mimicked the uncoupling action of Ca2+. The presence of a metabolic inhibitor alone had no effect on the coupling. These results lead to the following conclusions: (i) Uncoupling is due to an increased free Ca2+ concentration at the junctions. (ii) The liberation of endogenous sequestered Ca2+ is not sufficient to produce uncoupling except if an excess Ca2+ had been previously sequestered. The electrical synapses in the buccal ganglion of Navanax thus appear to be affected by Ca2+ in a similar way as gap junctions studied in non-neural tissues.
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1. Those features of a transmembrane current correlated with spike initiation were examined in Aplysia neurones using a Gaussian white-noise stimulus. This stimulus has the advantages that it presents numerous wave forms in random order without prejudgement as to their efficacies, and that it allows straightforward statistical calculations. 2. Stimulation with a repeating segment of Gaussian white-noise current revealed remarkable invariance in the firing times of the tested neurones and indicated a high degree of reliability of their response. 3. Frequencies (less than 5 Hz) involved in spike triggering propagated faithfully for up to several millimetres, justifying intrasomatic current injection to examine spike initiation at the trigger locus. 4. Examination of current wave forms preceding spikes indicated that a wide variety could be effective. Hence, a statistical analysis was performed, including computation of probability densities, averages, standard deviations and correlation coefficients of pairs of current values. Each statistic was displayed as a function of time before the spike. 5. The average current trajectory preceding a spike was multiphasic and depended on the presence and polarity of a d.c. bias. An early relatively small inward- or outward-going phase was followed by a large outward phase before the spike. The early phase tended to oppose the polarity of the d.c. bias. 6. The late outward phase of the average current trajectory reached a maximum 40--75 msec before triggering the action potential (AP) and returned to near zero values at the moment of triggering. The fact that the current peak occurs in advance of the AP may be partially explained by a phase delay between the transmembrane current and potential. The failure of the average current trajectory to return to control values immediately following the peak argues for a positive role of the declining phase in spike triggering. 7. Probability densities preceding spikes were Gaussian, indicating that the average was also the most probable value. Although the densities were broad, confirming that spikes were preceded by a wide variety of current wave forms, their standard deviations were reduced significantly with respect to controls, suggesting preferred status of the average current trajectory in spike triggering. 8. The matrix of correlation coefficients between current pairs suggested that spikes tended to be preceded by wave forms that in part kept close to the average current trajectory and in part preserved its shape. 9. The average first and second derivatives of spike-evoking epochs revealed that current slope and acceleration, respectively, were most crucial in the last 200 msec before spike triggering, and that these dynamic stimulus components were more important for a cell maintained under a depolarizing, rather than a hyperpolarizing bias. 10...
1. The spike discharges of single first order afferents from the utricle were recorded in the isolated head of the guitarfish and tested for responses to maintained spatial orientation, to transitions and to a small positional jitter representing natural perturbations. Sensitivity to maintained orientation is referred to as "tonic", and to transitions and jitter as "phasic". 2. Most responsive cells were either phasically, or phasically and tonically sensitive. A few were exclusively tonic. Tonic responsiveness implied that maintained orientation was associated with a stationary discharge which differed from one position to another; it sometimes differed also from one station to another at the same position. Transitions from one position to another evoked a rate change that later adapted to the level of the tonic response. Opposite transitions evoked rate changes in the opposite sense. The phasic rate change was usually larger for transitions that increased the rate. Many units were non-responsive. The prevalence of phasic over tonic sensitivity is stressed, and the remarkable heterogeneity of utricular afferents confirms that the macula is not uniform, probably coding a wide variety of head accelerations. 3. The jitter increased the ongoing scatter of intervals and binrates, changing, complicating, or abolishing their periodicity. The jitter could influence the effects of maintained orientation, increasing, decreasing, inverting or even revealing directional sensitivity. It could also force previously independent units into an orientation-dependent correlation; hence, between-cell correlation is potentially useful in coding of spatiel orientation. Naturally occurring perturbations may sonstitute a significant issue of normal operation. 4. Certain afferents from the horizontal semicircular canal showed a slow tonic response to maintained spatial orientation.
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The influence of basic open-loop synaptic connections on the firing of simultaneously recorded neurons has been investigated with auto- and cross-correlation histograms, using experimental records and computer simulations. The basic connections examined were direct synaptic excitation, direct synaptic inhibition, and shared synaptic input. Each type of synaptic connection produces certain characteristic features in the cross-correlogram depending on the properties of the synapse and statistical features in the firing pattern of each neuron. Thus, empirically derived cross-correlation measures can be interpreted in terms of the underlying physiological mechanisms. Their potential uses and limitations in the detection and identification of synaptic connections between neurons whose extracellularly recorded spike trains are available are discussed.
The opisthobranch mollusc, Navanax, is carnivorous and cannibalistic. Prey are swallowed whole by way of a sudden expansion of the pharynx. The buccal ganglion which controls this sucking action was isolated and bathed in seawater. Attention was focused upon 10 identifiable cells visible on the ganglion's rostral side. Two cells were observed simultaneously, and each was penetrated with two glass microelectrodes, one for polarizing the membrane and the other for recording membrane potential variations. The coupling coefficients for direct current flow and action potentials of several identified cells were tabulated. Attenuation was essentially independent of the direction of current flow, but depended upon the relative size of the directly and indirectly polarized cells. The attenuation of subthreshold sinusoidally varying voltages increased with frequency above about 1 Hz. The coupling coefficient for spikes was lower than for DC due to greater high frequency attenuation. There is considerable similarity in the spontaneous PSP's of all cells, which is not due to the electrical coupling but to input from a common source. The 10 cells were not chemically interconnected but some were electrically connected to interneurons which fed back chemically mediated PSP's. The feedback can be negative or positive depending upon the membrane potential of the postsynaptic cell. We conclude that electrical coupling among the 10 cells plays a minor role in sudden pharyngeal contractions but that the dual electrical-chemical coupling with interneurons may be important in this respect.
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