Physiological properties of types of intercellular junctions in the nervous system.
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Biomedical subjects
Publications and source records attributed to M V Bennett.
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The dye Procion Yellow M4RS crosses junctional membranes from cytoplasm to cytoplasm at electrotonic synapses between segments of the crayfish septate axon. The dye does not enter the cells from extracellular space. Thus permeability of junctional membranes is qualitatively different from that of nonjunctional membranes. Electron microscopy after fixation in the presence of lanthanum hydroxide indicates that these synapses are "gap junctions" and that there is a network of channels continuous with extracellular space between apposed junctional membranes. These channels must be interlaced with intercytoplasmic channels that are not open to extracellular space.
Oculomotor neurons are electrotonically coupled in three teleosts. Electron microscopy revealed axosomatic synapses with close appositions of pre- and postynaptic membranes. Similar junctions are associated with electrotonic coupling in many other cases. Stimulation of the ipsilateral eighth nerve usually initiated impulses at sites distant from the cell bodies; stimulation of the ipsilateral ophthalmic nerve initiated impulses close to the cell bodies. Electrotonic coupling may synchronize impulses arising near the, cell bodies to generate synchronous muscle contractions. Impulses arising distant from the cell bodies may lead to contractions of graded strength.
The junctional resistance at septa of the crayfish lateral giant axon is inversely related to temperature with a Q(1l), of about 3 over the range from 5 degrees to 20 degrees C. Nonjunctional axonal membrane is much less affected. Resistance changes occur rapidly with temperature changes. No correlates in ultrastructure of the synapses have been found.
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The hatchetfish, Gasteropelecus, possesses large pectoral fin adductor muscles whose simultaneous contraction enables the fish to dart upwards at the approach of a predator. These muscles can be excited by either Mauthner fiber. In the medulla, each Mauthner fiber forms axo-axonic synapses on four "giant fibers," two on each side of the midline. Each pair of giant fibers innervates ipsilateral motoneurons controlling the pectoral fin adductor muscles. Mauthner fibers and giant fibers can be penetrated simultaneously by microelectrodes close to the synapses between them. Electrophysiological evidence indicates that transmission from Mauthner to giant fiber is chemically mediated. Under some conditions miniature postsynaptic potentials (PSP's) are observed, suggesting quantal release of transmitter. However, relatively high frequency stimulation reduces PSP amplitude below that of the miniature potentials, but causes no complete failures of PSP's. Thus quantum size is reduced or postsynaptic membrane is desensitized. Ramp currents in Mauthner fibers that rise too slowly to initiate spikes can evoke responses in giant fibers that appear to be asynchronous PSP's. Probably both spikes and ramp currents act on the same secretory mechanism. A single Mauthner fiber spike is followed by prolonged depression of transmission; also PSP amplitude is little affected by current pulses that markedly alter presynaptic spike height. These findings suggest that even a small spike releases most of an immediately available store of transmitter. If so, the probability of release by a single spike is high for any quantum of transmitter within this store.
The adductor muscles of the pectoral fins of the hatchetfish Gasteropelecus are innervated by bilateral pools of about 40 motoneurons which lie primarily in the first spinal segment. A pair of giant fibers on each side of the medulla send processes ventroposteriorly to the motoneuron pools. Electrophysiological evidence indicates that giant fibers are presynaptic to ipsilateral motoneurons, but not to contralateral ones. Transmission across the giant fiber, motoneuron synapse is electrically mediated as is indicated by direct measurement of electrotonic spread in either direction across the synapse, and by the extremely short latency of the giant fiber postsynaptic potentials (PSP's) in the motoneuron. The coupling resistance across the synapse was calculated from measurements of input and transfer resistance. The coupling resistance rectifies in such a way as to facilitate spread of depolarization from giant fiber to motoneuron, and to oppose transmission in the opposite direction. As a consequence of rectification, the giant fiber PSP in a motoneuron is augmented by hyperpolarization of the motoneuron. The coupling resistance calculated on the basis of this effect is in good agreement with calculations from input and transfer resistance data. Rectification at the electrotonic synapses may permit the motoneurons to act in small swimming movements as well as to fire synchronously in an extremely fast escape reflex mediated by Mauthner and giant fibers.
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In electroplaques of several gymnotid fishes hyperpolarizing or depolarizing currents can evoke all-or-none responses that are due to increase in membrane resistance as much as 10- to 12-fold. During a response the emf of the membrane shifts little, if at all, when the cell either is at its normal resting potential, or is depolarized by increasing external K, and in the case of depolarizing responses when either Cl or an impermeant anion is present. Thus, the increase in resistance is due mainly, or perhaps entirely, to decrease in K permeability, termed depolarizing or hyperpolarizing K inactivation, respectively. In voltage clamp measurements the current-voltage relation shows a negative resistance region. This characteristic accounts for the all-or-none initiation and termination of the responses demonstrable in current clamp experiments. Depolarizing inactivation is initiated and reversed too rapidly to measure with present techniques in cells in high K. Both time courses are slowed in cells studied in normal Ringer's. Once established, the high resistance state is maintained as long as an outward current is applied. Hyperpolarizing inactivation occurs in normal Ringer's or with moderate excess K. Its onset is more rapid with stronger stimuli. During prolonged currents it is not maintained; i.e., there is a secondary increase in conductance. Hyperpolarizing inactivation responses exhibit a long refractory period, presumably because of persistence of this secondary increase in conductance.
Weakly electric fish of the African family Mormyridae emit pulses at variable intervals with a distribution skewed toward longer intervals. Fourteen specimens of the genera Mormyrops, Gnathonemus, and Marcusenius were classically conditioned to increase briefly their discharge frequency. The unconditioned stimulus was electric shock and the conditioned stimulus was light. These results are novel in that the overt conditioned response involves neither secretion nor movement.
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