Neural repetitive firing: a comparative study of membrane properties of crustacean walking leg axons

Connor, J. A.

doi:10.1152/jn.1975.38.4.922

Cited by 79 publications

(54 citation statements)

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“…The strong anti-Shaker staining observed in the distal membranes of most axons suggests that Shaker channels contribute to spike propagation in pyloric neurons, as is true for Shaker channels in a variety of species (Wang et al, 1993;Rosenthal et al, 1996Rosenthal et al, , 1997Rogero et al, 1997). This observation is consistent with the fact that both sustained and transient K ϩ currents exist in lobster axons (Connor, 1975). Interestingly, Shaker channel distribution is not uniform along an axon, and Shaker channels are missing from the proximal regions.…”

Section: Shaker and Shal Contribute To Distinct Firing Properties Witsupporting

confidence: 60%

Molecular Underpinnings of Motor Pattern Generation: Differential Targeting of Shal and Shaker in the Pyloric Motor System

et al. 2000

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The patterned activity generated by the pyloric circuit in the stomatogastric ganglion of the spiny lobster, Panulirus interruptus, results not only from the synaptic connectivity between the 14 component neurons but also from differences in the intrinsic properties of the neurons. Presumably, differences in the complement and distribution of expressed ion channels endow these neurons with many of their distinct attributes. Each pyloric cell type possesses a unique, modulatable transient potassium current, or A-current (I A ), that is instrumental in determining the output of the network. Two genes encode A-channels in this system, shaker and shal. We examined the hypothesis that cellspecific differences in shaker and shal channel distribution contribute to diversity among pyloric neurons. We found a stereotypic distribution of channels in the cells, such that each channel type could contribute to different aspects of the firing properties of a cell. Shal is predominantly found in the somatodendritic compartment in which it influences oscillatory behavior and spike frequency. Shaker channels are exclusively localized to the membranes of the distal axonal compartments and most likely affect distal spike propagation. Neither channel is detectably inserted into the preaxonal or proximal portions of the axonal membrane. Both channel types are targeted to synaptic contacts at the neuromuscular junction. We conclude that the differential targeting of shaker and shal to different compartments is conserved among all the pyloric neurons and that the channels most likely subserve different functions in the neuron.

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Section: Shaker and Shal Contribute To Distinct Firing Properties Witsupporting

confidence: 60%

Molecular Underpinnings of Motor Pattern Generation: Differential Targeting of Shal and Shaker in the Pyloric Motor System

et al. 2000

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“…Activation of 'A opposes depolarization and lengthens the time to the threshold of spike. It has been concluded that a frequency-encoding function in these cells is attributable to these characteristics of IA (Connor, 1975(Connor, , 1980. On the other hand, 'A-like current in cardiac cells has been reported as a current responsible for the early repolarization of action potentials (Josephson et al 1984;Giles & van Ginneken, 1985;.…”

Section: Effects Of Divalent Cations On Itomentioning

confidence: 99%

Characteristics of transient outward currents in single smooth muscle cells from the ureter of the guinea‐pig.

Imaizumi

Muraki

Watanabe

1990

The Journal of Physiology

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4. Single-channel outward currents which appeared only in the initial part of a depolarizing pulse from about -100 mV were recorded using the cell-attached patch clamp. The decay of the ensemble average of the current was similar to the macroscopic ITO under whole-cell clamp. When the holding potential was less negative, the opening probability of the channel greatly decreased. The channel conductance in normal extracellular medium was 14 pS.5. In ureter cells ITO resembles A-type current. ITO does not contribute

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“…Experimentally, this means the frequency-input current (or FI) curve has a specific shape, called Type I, such that firing frequency smoothly approaches zero at current threshold (1-6). By contrast, so-called Type II neurons have a lower bound in their firing frequency and move abruptly from quiescence to fast spiking, with this transition visible as a sharp jump in the FI curve at threshold (1,3,5).Type I behavior is physiologically unlikely with a minimal set of membrane currents such as the voltage-gated sodium and delayed-rectifier potassium currents in the standard squid giant axon Hodgkin-Huxley model, which is Type II. Classic experimental (1, 7) and theoretical studies (3-5, 8, 9) revealed that a Type II membrane (such as a squid giant axon) can be turned into a Type I membrane by adding an inactivating (A-type) potassium conductance, I A .…”

mentioning

confidence: 99%

“…For a neuron to represent continuously varying signals in its firing rate, it must be able to fire at low, high, and all intermediate frequencies. Experimentally, this means the frequency-input current (or FI) curve has a specific shape, called Type I, such that firing frequency smoothly approaches zero at current threshold (1)(2)(3)(4)(5)(6). By contrast, so-called Type II neurons have a lower bound in their firing frequency and move abruptly from quiescence to fast spiking, with this transition visible as a sharp jump in the FI curve at threshold (1,3,5).…”

mentioning

confidence: 99%

“…Classic experimental (1,7) and theoretical studies (3-5, 8, 9) revealed that a Type II membrane (such as a squid giant axon) can be turned into a Type I membrane by adding an inactivating (A-type) potassium conductance, I A . As the density of I A channels increases from zero, the membrane is able to support progressively lower firing frequencies at spiking threshold.…”

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confidence: 99%

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Ion channel degeneracy enables robust and tunable neuronal firing rates

Drion

O’Leary

Marder

2015

Proc. Natl. Acad. Sci. U.S.A.

129

165

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Firing rate is an important means of encoding information in the nervous system. To reliably encode a wide range of signals, neurons need to achieve a broad range of firing frequencies and to move smoothly between low and high firing rates. This can be achieved with specific ionic currents, such as A-type potassium currents, which can linearize the frequency-input current curve. By applying recently developed mathematical tools to a number of biophysical neuron models, we show how currents that are classically thought to permit low firing rates can paradoxically cause a jump to a high minimum firing rate when expressed at higher levels. Consequently, achieving and maintaining a low firing rate is surprisingly difficult and fragile in a biological context. This difficulty can be overcome via interactions between multiple currents, implying a need for ion channel degeneracy in the tuning of neuronal properties.FI curve | bifurcation | Type I excitability | Type II excitability | reduced neuron model F iring rates encode the intensities of many signals in the nervous system, whether these are inputs from sensory organs, internal representations of percepts, or muscle contraction commands in motor nerves. For a neuron to represent continuously varying signals in its firing rate, it must be able to fire at low, high, and all intermediate frequencies. Experimentally, this means the frequency-input current (or FI) curve has a specific shape, called Type I, such that firing frequency smoothly approaches zero at current threshold (1-6). By contrast, so-called Type II neurons have a lower bound in their firing frequency and move abruptly from quiescence to fast spiking, with this transition visible as a sharp jump in the FI curve at threshold (1,3,5).Type I behavior is physiologically unlikely with a minimal set of membrane currents such as the voltage-gated sodium and delayed-rectifier potassium currents in the standard squid giant axon Hodgkin-Huxley model, which is Type II. Classic experimental (1, 7) and theoretical studies (3-5, 8, 9) revealed that a Type II membrane (such as a squid giant axon) can be turned into a Type I membrane by adding an inactivating (A-type) potassium conductance, I A . As the density of I A channels increases from zero, the membrane is able to support progressively lower firing frequencies at spiking threshold. The resulting linearization of the FI curve from Type II to Type I has clear consequences for encoding information in firing rate as well as other computational properties such as thresholding and gain scaling, all of which are subjects of intense research (10-17).We now show that this picture is incomplete. Using rigorous but intuitive methods (18) and building on previous technical results (19-21), we show that introducing I A to a Type II neuron progressively linearizes but then delinearizes the FI curve as I A density increases further. Consequently, I A density must be tuned in a strict range to achieve Type I behavior. However, we show that other, unrelated currents including v...

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Neural repetitive firing: a comparative study of membrane properties of crustacean walking leg axons

Cited by 79 publications

References 0 publications

Molecular Underpinnings of Motor Pattern Generation: Differential Targeting of Shal and Shaker in the Pyloric Motor System

Molecular Underpinnings of Motor Pattern Generation: Differential Targeting of Shal and Shaker in the Pyloric Motor System

Characteristics of transient outward currents in single smooth muscle cells from the ureter of the guinea‐pig.

Ion channel degeneracy enables robust and tunable neuronal firing rates

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