Changes in Electrophysiological Properties of Lamprey Spinal Motoneurons During Fictive Swimming

2002 ◽  
Vol 88 (5) ◽  
pp. 2463-2476 ◽  
Author(s):  
Michelle M. Martin

Electrophysiological properties of lamprey spinal motoneurons were measured to determine whether their cellular properties change as the spinal cord goes from a quiescent state to the active state of fictive swimming. Intracellular microelectrode recordings of membrane potential were made from motoneurons in the isolated spinal cord preparation. Electrophysiological properties were first characterized in the quiescent spinal cord, and then fictive swimming was induced by perfusion with d-glutamate and the measurements were repeated. During the depolarizing excitatory phase of fictive swimming, the motoneurons had significantly reduced rheobase and significantly increased input resistance compared with the quiescent state, with no significant changes in these parameters during the repolarizing inhibitory phase of swimming. Spike threshold did not change significantly during fictive swimming compared with the quiescent state. During fictive swimming, the slope of the spike frequency versus injected current ( F-I) relationship decreased significantly as did spike-frequency adaptation and the amplitude of the slow after-spike hyperpolarization (sAHP). Serotonin is known to be released endogenously from the spinal cord during fictive swimming and is known to reduce the amplitude of the sAHP. Therefore the effects of serotonin on cellular properties were tested in the quiescent spinal cord. It was found that, in addition to reducing the sAHP amplitude, serotonin also reduced the slope of the F-I relationship and reduced spike-frequency adaptation, reproducing the changes observed in these parameters during fictive swimming. Application of spiperone, a serotonin antagonist, significantly increased the sAHP amplitude during fictive swimming but had no significant effect on F-I slope or adaptation. Because serotonin may act in part through reduction of calcium currents, the effect of calcium-free solution (cobalt substituted for calcium) was tested in the quiescent spinal cord. Similar to fictive swimming and serotonin application, the calcium-free solution significantly reduced the sAHP amplitude, the slope of the F-I relationship, and spike-frequency adaptation. These results suggest that there are significant changes in the firing properties of motoneurons during fictive swimming compared with the quiescent state, and it is possible that these changes may be attributed in part to the endogenous release of serotonin acting via reduction of calcium currents.

2011 ◽  
Vol 105 (3) ◽  
pp. 1045-1050 ◽  
Author(s):  
Robert M. Brownstone ◽  
Sherry Krawitz ◽  
Larry M. Jordan

In spinal motoneurons, late spike frequency adaptation (SFA) is defined as the slowing of the firing rate over tens of seconds and can be seen during sustained or intermittent current injection. Although the function of late SFA is not known, it may result in a decrease in force production over time, or muscle fatigue. Because locomotion can persist for long periods of time without fatigue, late SFA was studied using intracellular recordings from adult cat motoneurons during fictive locomotion. Of eight lumbar motoneurons studied, all showed late adaptation during control conditions, but none demonstrated late adaptation during locomotor activity. The most consistent properties that correlated with the presence or absence of late SFA were those related to availability of fast, inactivating sodium channels, particularly action potential rate of rise. Evidence of the reversal of late SFA during locomotion was present for several minutes following locomotor trials, consistent with the suggestion that SFA is modulated through slow metabotropic pathways. The abolition of late adaptation in spinal motoneurons during fictive locomotion is an example of a state-dependent change in the “intrinsic” properties of mammalian motoneurons. This change contributes to increased excitability of motoneurons during locomotion and results in robust firing during sustained locomotion.


2004 ◽  
Vol 91 (5) ◽  
pp. 1963-1980 ◽  
Author(s):  
Charles J. Wilson ◽  
Angela Weyrick ◽  
David Terman ◽  
Nicholas E. Hallworth ◽  
Mark D. Bevan

Subthalamic nucleus neurons exhibit reverse spike-frequency adaptation. This occurs only at firing rates of 20–50 spikes/s and higher. Over this same frequency range, there is an increase in the steady-state frequency–intensity ( F– I) curve's slope (the secondary range). Specific blockade of high-voltage activated calcium currents reduced the F– I curve slope and reverse adaptation. Blockade of calcium-dependent potassium current enhanced secondary range firing. A simple model that exhibited these properties used spike-triggered conductances similar to those in subthalamic neurons. It showed: 1) Nonaccumulating spike afterhyperpolarizations produce positively accelerating F– I curves and spike-frequency adaptation that is complete after the second spike. 2) Combinations of accumulating aftercurrents result in a linear F– I curve, whose slope depends on the relative contributions of inward and outward currents. Spike-frequency adaptation can be gradual. 3) With both accumulating and nonaccumulating aftercurrents, primary and secondary ranges will be present in the F– I curve. The slope of the primary range is determined by the nonaccumulating conductance; the accumulating conductances govern the secondary range. The transition is determined by the relative strengths of accumulating and nonaccumulating currents. 4) Spike-threshold accommodation contributes to the secondary range, reducing its slope at high firing rates. Threshold accommodation can stabilize firing when inward aftercurrents exceed outward ones. 5) Steady-state reverse adaptation results when accumulated inward aftercurrents exceed outward ones. This requires spike-threshold accommodation. Transient speedup arises when inward currents are smaller than outward ones at steady state, but accumulate more rapidly. 6) The same mechanisms alter firing in response to irregular patterns of synaptic conductances, as cell excitability fluctuates with changes in firing rate.


2004 ◽  
Vol 92 (1) ◽  
pp. 327-340 ◽  
Author(s):  
Raymon M. Glantz ◽  
John P. Schroeter

The responses of sustaining and dimming fibers were characterized by the time varying firing rates elicited by extrinsic current and flashes of light. These data were simulated by an adaptive integrate-and-fire model. A postimpulse shunt conductance simulated spike-frequency adaptation. The correlation between observed and model current-elicited impulse rates was 0.94–0.98. However, except for a difference in input resistance (both measured and simulated), the voltage to impulse encoders of the two cell groups was similar and exhibited comparable degrees of spike-frequency adaptation (40 to 45%). The encoder model derived from current-elicited responses (with fixed parameters) was used to simulate visual responses elicited by light flashes. These simulations included a synaptic current derived from the time course of the postsynaptic potential (PSP). The sustaining fiber visual response consisted of a large excitatory PSP and high-frequency transient burst that adapted (by ∼80%) to a low-frequency plateau discharge. The simulations indicated that spike-frequency adaptation had no effect on the transient discharge but reduced the plateau firing rate by ∼60%. Encoder adaptation enhances the sustaining fiber response to the time derivative of the stimulus. In dimming fibers, the light flash elicits an inhibitory PSP that interrupts the “dark discharge” and an off response following the end of the flash. The simulations indicated that spike-frequency adaptation reduces the firing rate of both the dark discharge and the off response. Thus the model suggests that different effects of encoder adaptation on the two cell types arise from the same encoder mechanisms, but different actions are determined by differences in impulse rate and the time course of the discharge.


2003 ◽  
Vol 15 (11) ◽  
pp. 2523-2564 ◽  
Author(s):  
Jan Benda ◽  
Andreas V. M. Herz

Spike-frequency adaptation is a prominent feature of neural dynamics. Among other mechanisms, various ionic currents modulating spike generation cause this type of neural adaptation. Prominent examples are voltage-gated potassium currents (M-type currents), the interplay of calcium currents and intracellular calcium dynamics with calcium-gated potassium channels (AHP-type currents), and the slow recovery from inactivation of the fast sodium current. While recent modeling studies have focused on the effects of specific adaptation currents, we derive a universal model for the firing-frequency dynamics of an adapting neuron that is independent of the specific adaptation process and spike generator. The model is completely defined by the neuron's onset f-I curve, the steady-state f-I curve, and the time constant of adaptation. For a specific neuron, these parameters can be easily determined from electrophysiological measurements without any pharmacological manipulations. At the same time, the simplicity of the model allows one to analyze mathematically how adaptation influences signal processing on the single-neuron level. In particular, we elucidate the specific nature of high-pass filter properties caused by spike-frequency adaptation. The model is limited to firing frequencies higher than the reciprocal adaptation time constant and to moderate fluctuations of the adaptation and the input current. As an extension of the model, we introduce a framework for combining an arbitrary spike generator with a generalized adaptation current.


2006 ◽  
Vol 96 (6) ◽  
pp. 2951-2962 ◽  
Author(s):  
Fabrizio Gabbiani ◽  
Holger G. Krapp

We investigated in vivo the characteristics of spike-frequency adaptation and the intrinsic membrane properties of an identified, looming-sensitive interneuron of the locust optic lobe, the lobula giant movement detector (LGMD). The LGMD had an input resistance of 4–5 MΩ, a membrane time constant of about 8 ms, and exhibited inward rectification and rebound spiking after hyperpolarizing current pulses. Responses to depolarizing current pulses revealed the neuron's intrinsic bursting properties and pronounced spike-frequency adaptation. The characteristics of adaptation, including its time course, the attenuation of the firing rate, the mutual dependency of these two variables, and their dependency on injected current, closely followed the predictions of a model first proposed to describe the adaptation of cat visual cortex pyramidal neurons in vivo. Our results thus validate the model in an entirely different context and suggest that it might be applicable to a wide variety of neurons across species. Spike-frequency adaptation is likely to play an important role in tuning the LGMD and in shaping the variability of its responses to visual looming stimuli.


2001 ◽  
Vol 85 (2) ◽  
pp. 714-723 ◽  
Author(s):  
E.S.L. Faber ◽  
R. J. Callister ◽  
P. Sah

In this study, we characterize the electrophysiological and morphological properties of spiny principal neurons in the rat lateral amygdala using whole cell recordings in acute brain slices. These neurons exhibited a range of firing properties in response to prolonged current injection. Responses varied from cells that showed full spike frequency adaptation, spiking three to five times, to those that showed no adaptation. The differences in firing patterns were largely explained by the amplitude of the afterhyperpolarization (AHP) that followed spike trains. Cells that showed full spike frequency adaptation had large amplitude slow AHPs, whereas cells that discharged tonically had slow AHPs of much smaller amplitude. During spike trains, all cells showed a similar broadening of their action potentials. Biocytin-filled neurons showed a range of pyramidal-like morphologies, differed in dendritic complexity, had spiny dendrites, and differed in the degree to which they clearly exhibited apical versus basal dendrites. Quantitative analysis revealed no association between cell morphology and firing properties. We conclude that the discharge properties of neurons in the lateral nucleus, in response to somatic current injections, are determined by the differential distribution of ionic conductances rather than through mechanisms that rely on cell morphology.


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