 |
||||
|
||||
|
||||
|
||||
The Journal of Neuroscience, August 20, 2003, 23(20):7461-7469
Previous Article | Next Article
Spike Width Reduction Modifies the Dynamics of Short-Term Depression at a Central Synapse in the Locust
J. E. Niven andM. Burrows Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom
Abstract
Top
Abstract
Introduction
Short-term synaptic depression is an important component of computation within neural networks, but little is known of its contribution to information processing during synaptically generated spike trains. We analyzed short-term synaptic depression at a synapse between two identified motoneurons innervating the hind leg of the locust: the FETi-FlTi synapse (fast extensor tibiae-flexor tibiae). Brief electrical stimulation of a single hind leg proprioceptor, the lump receptor (LR), led to prolonged sequences of spikes in FETi, similar in number and frequency to those during natural kicking movements. Depression at the FETi-FlTi synapse during LR-evoked spike bursts was compared quantitatively to that during antidromic spike trains evoked by electrical stimulation of FETi in the extensor tibiae muscle, and by modeling. The magnitude of the short-term depression was significantly greater during LR-evoked spike trains. On the basis of the model parameters required to fit the depression, the FETi-FlTi synapse is predominantly used for transmitting the timing of the onset of FETi spiking rather than its spike rate. During LR-evoked spike trains, there was a rapid reduction in presynaptic spike width that did not occur during antidromic spike trains under physiological calcium concentrations. This produced a concomitant reduction in the amplitude of the FlTi EPSP, suggesting that it contributed to the differences between the two stimulation regimes. Differences in the short-term depression between synaptically evoked and antidromic spike trains emphasize that the properties of synaptic information transfer are dependent on the in vivo conditions at the synapse and may not be reproduced by in vitro spike trains.
Key words: synaptic depression; motor control; proprioception; Schistocerca gregaria; lump receptor; presynaptic waveform; presynaptic inhibition
Introduction
Many chemical synapses undergo short-term frequency-dependent changes in their efficacy, resulting in depression or facilitation (Eccles et al., 1941; Feng, 1941
A monosynaptic connection exists between the fast motoneuron (FETi) innervating the extensor tibiae muscle of the hind leg of the locust and the flexor motoneurons (FlTi) innervating the antagonistic flexor tibiae muscle (Hoyle and Burrows, 1973
Stimulation of a particular joint proprioceptor, the lump receptor (LR) (Heitler and Burrows, 1977
Materials and Methods
Preparation and electrophysiology. Adult desert locusts (Schistocerca gregaria; Forskål) of either sex were taken from a crowded colony maintained in the Department of Zoology, University of Cambridge. They were mounted ventral surface uppermost in modeling clay (Plasticine), and the femur and tibia of each leg was fully restrained, with the exception of the tibia of the left hind leg, which was able to extend fully. During experiments in which the lateral nerve (LN), or one of its branches, which contain the axons of the LR, was stimulated, the tibia was not allowed to flex to angles of <20° to prevent damage to stimulation electrodes. The metathoracic ganglion was exposed by cutting a window in the ventral thorax and removing surrounding air sacs while leaving the main trachae intact. The mesothoracic and metathoracic ganglia were stabilized on a wax-coated silver platform to prevent movement during the experiment. The thorax was continually perfused with physiological saline (Usherwood and Grundfest, 196545 sec to facilitate penetration with thick-walled borosilicate glass microelectrodes (40-80 M
) filled with 2 M potassium acetate.
A window was cut into the ventral posterior surface of the distal femur to reveal the LN, which was recorded or stimulated extracellularly with two 100 µm silver hook electrodes. The electrodes were placed either on the whole nerve or on the nerve branch innervating only the lump receptor (LRN). This allowed the LR to be stimulated independently of other F-T joint proprioceptors. Electrical stimulation (0.5-1 msec; 120% of threshold) of the LN or LRN at 7Hz or more (up to 50Hz) reliably evoked bursts of spikes in FETi that continue beyond the duration of the stimulation. Stimulation was stopped once a burst of spikes was evoked, and sequential bursts were evoked at least 2 min apart to enable the FETi-FlTi synapse to recover fully after a spike burst.
Intracellular recordings were made from motoneurons controlling tibial extension and flexion, which were identified in the following ways: electrical stimulation of the extensor muscle with a pair of 50 µm steel wires excited the peripheral terminals of FETi and evoked an antidromic spike. Flexor motoneurons were identified by a short latency monosynaptic EPSP that followed each antidromic FETi spike (Hoyle and Burrows, 1973
Intracellular recordings were stored on a Racal FM tape recorder and were subsequently analyzed offline using a Cambridge Electronic Design A/D conversion interface and Spike 2 software. All statistical tests were performed using MINITAB and Microsoft Excel. The results are based on 46 recordings from 33 animals. Here, N refers to the number of animals used and n to the number of repeats within a single animal.
Analysis and modeling. The model used to characterize depression at the FETi-FlTi synapse was based on the three-parameter model proposed by Tsodyks and Markram (1997
Rec). The model is formulated so that after a spike, a fraction (U) of the absolute amount of transmitter available (A) is released that evokes an EPSP in the postsynaptic neuron. The released transmitter is unavailable to subsequent spikes and recovers with a time constant of
Additional parameters were added to determine any possible effects of underlying facilitation on the depression at the FETi-FlTi synapse. U applies only to the first spike in a train, and u is the updated value of U. The updated value of u incorporates facilitation at the synapse via a single exponential,
The transmitter released after the first spike is A*U and R0 = 1, because the maximum amount of transmitter is stored before the spike. Immediately after this spike, the remaining transmitter is r = 1 - U, and at the occurrence of the next spike, the remaining transmitter will be this plus the amount of transmitter recovered. Hence, the amount of transmitter remaining is dependent on the timing of subsequent spikes and is:
where
t is the time interval between the nth and (n + 1)th AP where:
During spike trains in which there is no contribution from facilitation
Data fitting. Only FlTi motoneurons in which there were no discernable synaptic inputs (other than those inputs from FETi) during LR stimulation were used for analysis. EPSP amplitudes in all FlTi motoneurons were measured from the baseline to peak, reducing the trains of EPSPs to a series of amplitudes and times. Similarly, AP amplitude was measured from the baseline to peak, and its width at half height. Experimentally derived data were fitted by iterating the parameters (A, U, and
Results
Depression and recovery at the FETi-FlTi synapse during natural spike trains
Electrical stimulation of the nerve innervating the LR evoked prolonged spike trains in the single FETi that outlasted the duration of the stimulus (Fig. 1A). Simultaneous recordings of FETi and FlTi motoneurons showed that some FlTi motoneurons did not receive synaptic inputs after electrical stimulation of the LR (Fig. 1B). The LR-evoked FETi spike trains contained similar numbers of spikes with a similar frequency distribution to those occurring during kicking. The bursts typically lasted for 1-4 sec, with each burst consisting of 10-40 spikes at frequencies up to 70 Hz (cf. Burrows, 1995
View larger version (16K):
[in this window]
[in a new window]
Figure 1. Depression at the FETi-FlTi central synapse during synaptically evoked spike trains. A, Brief electrical stimuli applied to the LN evokes bursts of spikes in the FETi that continue after the termination of the stimuli. Spikes in FETi evoke an EPSP in antagonistic FlTi via a monosynaptic connection. Inset, A schematic of the circuit generating the bursts of spikes in FETi and their corresponding FlTi EPSPs. B, A single FETi spike evokes a monosynaptic EPSP in a FlTi. Stimulation of the LN evokes EPSPs in FETi (indicated by asterisk) that evoke spikes but does not evoke inputs to a subset of FlTi motoneurons, which receive inputs only from the FETi and not from local interneurons. C, A schematic diagram of the relative positions of input (black arrows) and output (gray arrows) synapses in FETi. Dashed lines indicate the resting potential in all traces.
During LR-evoked spike trains, the amplitude of the FlTi EPSPs depressed to
View larger version (28K):
[in this window]
[in a new window]
Figure 2. The dynamics of depression at the FETi-FlTi synapse during natural-like synaptically evoked spike trains. Ai, The FETi ISF and posterior fast FlTi EPSP amplitude corresponding to each spike during a burst. Aii, The mean (±SE) of 19 FFlTi motoneuron EPSPs during bursts of spikes in FETi fitted by a single exponential. The shaded area indicates the plateau region of the FETi ISF. B, The relationship between the FETi ISF and FlTi EPSP amplitude for a single FETi-FlTi pair (n = 6) could be fitted by a single exponential decay. C, The relationship between depression at the FETi-FlTi synapse and the initial FlTi EPSP amplitude. The level of depression after 15 spikes was dependent on the initial FlTi EPSP amplitude; depression was greater after larger initial EPSPs than after smaller initial EPSPs.
Frequency dependence of depression at the FETi-FlTi synapse
Figure 2B shows the relationship between ISF and the FlTi EPSP amplitude for three successive spike trains recorded from the a single FETi-FlTi pair. During the first four to six spikes (i.e., before the onset of the plateau phase), the frequency of FETi spikes accurately predicted the EPSP amplitude; spikes with similar ISFs occurred at similar times within each spike train, and they, therefore, contained information about the preceding number of spikes in the train and their interspike intervals. Once the ISF had plateaued, there was little or no further depression in the FlTi EPSP, and large fluctuations in the FETi ISF had little effect on EPSP amplitude (indicated by the flattening of the exponential decay in Fig. 2B).Depression at the FETi-FlTi synapse is dependent on the initial EPSP amplitude
Synaptic depression is often generated by presynaptic mechanisms that are affected by changes in the initial release probability (Zucker, 1989Comparison with depression during antidromic trains of spikes in FETi
Despite the differences in the waveform of antidromic and synaptically generated spikes in FETi (Gwilliam and Burrows, 1979), they evoked EPSPs with similar amplitudes and time courses in FlTi motoneurons (Fig. 3A). During antidromic stimulation at frequencies up to 70 Hz, the maximum spike frequency that occurred during LR-evoked spike trains, the level of depression at the FETi-FlTi synapse did not drop below 20% (20.36 ± 0.33%; N = 19; n = 10; mean ± SE) of the initial amplitude (Fig. 3B). The relationship between the antidromic spike frequency and the steady-state EPSP amplitude, at which there is no further reduction in EPSP amplitude, was fitted by a single exponential with a rate constant of 6.21 sec-1. Depression during antidromic spike trains never exceeded depression during synaptically generated spike trains, even when the frequency of the antidromic spikes was greater than the maximum frequency of synaptically generated spikes.
View larger version (20K):
[in this window]
[in a new window]
Figure 3. Depression at the FETi-FlTi synapse during antidromically generated spike trains. A, EPSPs evoked in FlTi motoneurons have similar amplitudes and durations after antidromic spikes (left) and synaptically generated spikes (right) in FETi. B, Steady-state EPSP amplitudes after depression at the FETi-FlTi synapse during antidromic spike trains in FETi calculated after the first 10 spikes (mean ± SD; N = 12; n = 10) fitted with a single exponential. Inset, Mean steady-state EPSP amplitudes at 0.5 and 5 Hz from a single FlTi motoneuron (n = 10).
Modeling short-term depression at the FETi-FlTi synapse
A model was used to compare the dynamics of depression at the FETi-FlTi synapse during synaptically and antidromically generated spike trains. The model produced an accurate fit of the depression at the FETi-FlTi synapse during a synaptically driven FETi spike burst (N = 1; n = 6) (Fig. 4A), shown by plotting the observed against the predicted EPSP amplitudes (Fig. 4B). The mean error in the fit of the model to LR-evoked spike trains was 0.16 ± 0.06 (N = 19; n = 6; for details of the calculation of the mean error, see Materials and Methods). To ensure that a more accurate fit could not be obtained from the model using additional parameters, a facilitation time constant was added. This produced only a small improvement in the fit (0.004 ± 0.0004) (Fig. 4C,D), suggesting that any underlying facilitating mechanisms make only a small contribution.
View larger version (28K):
[in this window]
[in a new window]
Figure 4. Modeling depression at the FETi-FlTi synapse during LR-evoked spike bursts. A, Averaged FlTi motoneuron responses during FETi spike bursts (n = 6) were fitted by a simple three-parameter model of synaptic depression (U = 0.61; A = 159.59;
The model was tested further by producing predictions to novel spike trains (individual spike trains) (Fig. 4E,F). Errors between the model predictions of novel LR-evoked spike trains and the observed EPSP amplitudes were greater than the errors in the fit of the model to specific data sets, although this increase in the error was small (0.05 ± 0.02) and fell within the variation in the fitted model spike trains (Fig. 4E,F, compare with Fig. 6B,D).
View larger version (28K):
[in this window]
[in a new window]
Figure 6. Modeling depression in multiple types of FlTi motoneurons. A, The model accurately average response of an intermediate FlTi motoneuron during FETi spike bursts but with different parameters to the PFFlTi motoneuron shown in Figure 4 (U = 0.72; A = 97.04;
For constant frequency antidromic spike trains, the model consistently predicted a faster rate of depression and a smaller EPSP amplitude for a given spike frequency than was observed (Fig. 5A,B). There was a significant increase in the mean error of model predictions for antidromic spike trains at frequencies above 10 Hz (0.99 ± 0.14; p < 0.001; N = 17; n = 10). To test whether the model could accurately fit the antidromic data, both with and without the additional facilitation parameter, it was allowed to iteratively fit the antidromic data (Fig. 5C-F). The model was then able to fit the antidromic spike trains, although its parameters were significantly different from those used to fit the LR-evoked spike trains (Fig. 5C,D). The addition of a facilitation parameter, as for the synaptically evoked spike trains, did not affect the fit of the model (Fig. 5E,F).
View larger version (30K):
[in this window]
[in a new window]
Figure 5. Model predictions do not fit observed antidromic spike trains. A, Parameters derived from fitting the model to FlTi responses during FETi spike bursts could not predict the responses of the same FlTi motoneurons to constant frequency antidromic spike trains at 20 Hz. B, Plotting the model against the data show the fit of the model to the data. Points lying on the diagonal indicate a perfect fit. C, The model could produce fits to constant frequency antidromic spike trains (U = 0.25; A = 394.31;
The model was able to fit the depression at the FETi-FlTi synapse for all types of FlTi motoneurons observed during simultaneous recordings and during sequential recordings, including both fast and intermediate FlTi motoneurons. The model parameters were unique for each FlTi motoneuron, although all of a particular class (e.g., fast FlTi motoneurons) had parameters clustered around similar values. Figure 6A-D shows two FlTi motoneurons recorded sequentially from the same preparation as the FlTi motoneuron in Figure 4. Two (Figs. 4, 6C,D) were fast FlTi motoneurons whereas the third (Fig. 6A,B) was an intermediate motoneuron. This suggests that, although there is some variation between FlTi motoneurons, the dynamics of depression at the FETi-FlTi synapse occurs within a restricted range.
One prediction made by the model is that if a presynaptic neuron spikes above a certain frequency, known as the limiting frequency, the amplitude of the EPSP evoked by each spike will decrease in proportion to the frequency (1/f). Therefore, above the limiting frequency, the mean postsynaptic depolarization from the resting potential saturates (i.e., as the spike frequency increases, the EPSP frequency increases but the individual EPSP amplitude decreases). Above the limiting frequency, increases in spike rate do not increase the mean level of depolarization in the postsynaptic neuron. Hence, the limiting frequency sets the frequency above which synapses are unable to transmit information about the presynaptic spike rate (Tsodyks and Markram, 1997
View larger version (17K):
[in this window]
[in a new window]
Figure 7. Predictions from the model suggest a behavioral role for depression at the FETi-FlTi synapse. A, Model predictions of steady-state EPSP amplitude fit a 1/f relationship for frequencies above 5 Hz (see Results for details). B, Model predictions of the steady-state EPSP amplitude for all the FlTi motoneurons analyzed. The gray lines indicate the upper and lower limits of the model predictions determined by the parameters for individual FlTi motoneurons, and the mean is shown by the bottom black line. The top black is the mean steady-state amplitude for a typical FlTi motoneuron during antidromic spike trains.
Presynaptic mechanisms
Changes in the height and width of the FETi spike were measured during synaptically evoked spike trains to determine whether changes in these parameters could account for the increased levels of depression relative to those during antidromic spike trains (Fig. 8A). The FETi spike height was reduced to
View larger version (34K):
[in this window]
[in a new window]
Figure 8. Changes in the presynaptic waveform during natural-like bursts of spikes in FETi. A, The spike height and width varied during synaptically evoked bursts of spikes in FETi. B, Three FETi spikes aligned at their onset show clear changes in both spike height and width. C, Correlation of the FETi spike height and width with the frequency of spiking during bursts of spikes as shown in A. D, Correlation of the FlTi EPSP amplitude with the FETi spike height and width during synaptically evoked bursts of spikes.
In antidromically induced trains of spikes, there was a smaller reduction in the FETi spike height to
View larger version (27K):
[in this window]
[in a new window]
Figure 9. Changes in the presynaptic waveform during antidromically generated spike trains in FETi. A, The steady-state spike height (black diamonds, calculated after the initial 10 spikes) and steady-state spike width (open circles) plotted against the antidromic spike frequency. Inset, The steady-state spike heights at 0.5 and 20 Hz. B, Relationship between the steady-state EPSP amplitude and the steady-state spike amplitude. The shaded region shows the plateau in the FlTi EPSP amplitude despite a continued drop in the FETi spike amplitude.
The FETi spike width during the synaptically evoked spike trains correlated strongly with the membrane potential of FETi immediately preceding a spike, increasing membrane potential leading to narrower spikes (Fig. 10A). To test whether changes in the width of synaptically evoked spikes had a causal effect on the FlTi EPSP, hyperpolarizing current was injected into FETi before the first spike of a LR-evoked spike train, increasing the spike width. The increased spike width and height produced a concomitant increase in the FlTi EPSP amplitude, implying a causal relationship between the presynaptic waveform and the FlTi EPSP (Fig. 10B). Reduction in the FETi spike width with increasing depolarization suggests that synaptic inputs may be responsible for this spike width modulation. Additionally, reduction in spike width could also be induced during antidromic spike trains by evoking synaptic inputs to FETi, providing evidence that synaptic inputs are sufficient to account for the differences in spike width between LR-evoked and antidromic spikes (Fig. 10C). This reduction in antidromic spike width was accompanied by a concomitant reduction in the amplitude of the FlTi EPSP (Fig. 10D), suggesting that the reduction in FETi spike width evoked by synaptic inputs is sufficient to generate the enhanced level of depression at the FETi-FlTi synapse during LR-evoked spike trains.
View larger version (20K):
[in this window]
[in a new window]
Figure 10. Spike width reduction during LR-evoked spike bursts may contribute to depression at the FETi-FlTi synapse. A, Changes in spike width correlate with changes in the depolarization of FETi immediately before the onset of the spike. B, Changes in the FETi spike height induced by injecting hyperpolarizing current produced a concomitant increase in the amplitude of the FlTi PSP. C, Three successive spikes during constant frequency antidromic spike trains synaptic inputs to FETi reduce the width of the antidromic spike. The second spike, which coincided with a synaptic input, has a reduced spike width. This trace is shifted (gray trace) to enable comparison with the other antidromic spikes. D, Antidromic spikes coinciding with synaptic inputs evoke smaller amplitude FlTi EPSPs.
Discussion
The importance of short-term depression in synaptic information transfer has been shown both experimentally and theoretically in many systems; yet despite this, the role of short-term depression during synaptically generated natural spike trains remains largely unknown. By making use of a circuit that transforms sensory input from a proprioceptor (LR) into a motor output, we have compared short-term depression elicited by synaptically or antidromically driven spike trains at a synapse between two identified motoneurons (FETi-FlTi synapse). The two stimulation regimes produced markedly different dynamics of short-term depression; during LR-evoked spike trains, both the rate and magnitude of depression was greater than during antidromic spike trains at similar spike frequencies. Moreover, the synaptic depression during LR-evoked spike trains could not be estimated from the antidromic, constant frequency spike trains.Several factors could have contributed to differences between the stimulation regimes, including the spiking statistics, spike waveform, or presence/absence of synaptic inputs. Modeling the depression at FETi-FlTi synapse showed that increased levels of depression during LR-evoked spike trains compared with antidromic spike trains were not because of the different spiking statistics. Additionally, despite differences in the overall shape of the spike waveform, single antidromically or synaptically generated spikes in FETi evoke similar amplitude EPSPs in FlTi motoneurons. This suggested that depolarizing synaptic inputs during LR-evoked spike trains in FETi were responsible for the increased depression at the FETi-FlTi synapse. Depolarizing synaptic inputs to FETi correlated with spike width changes during LR-evoked spike trains that did not occur during antidromic spike trains. Manipulating the FETi spike width showed that it contributed to FlTi EPSP amplitude and, therefore, may have contributed to the dynamics of short-term synaptic depression observed in FlTi motor neurons during LR-evoked spike trains.
How do synaptic inputs affect the efficacy of transmission at the FETi-FlTi synapse?
The presence of depolarizing synaptic inputs during LR-evoked spike trains correlates strongly with a 40% reduction in the FETi spike width. During constant frequency antidromic spike trains, there is only a 5% reduction in spike width under physiological conditions, suggesting that reduction in spike width may be responsible for the increased level of depression during LR-evoked spike trains. This is supported by two observations: (1) antidromic spike width is reduced in the presence of depolarizing synaptic inputs; and (2) FlTi EPSP amplitude is increased when FETi spike width is increased by hyperpolarizing current injection. Changes in spike width may affect the presynaptic calcium entry, thereby affecting the amount of neurotransmitter released at a synapse; small increases in spike width (Several possible mechanisms could explain the spike width reduction induced by synaptic inputs in FETi. Electron microscopy studies of the FETi-FlTi synapse have revealed that the input and output synapses in FETi are in close proximity in a region of neuropil that lacks voltage-gated Na+ channels (Gwilliam and Burrows, 1980
Presynaptic inputs may affect synaptic output via changes in the spike waveform in both vertebrate and invertebrate neural networks (Nusbaum et al., 1997
Mechanisms underlying depression and recovery at the FETi-FlTi synapse
Depletion of the releasable transmitter store explains many of the features of short-term depression at several synapses (Liley and North, 1953At the FETi-FlTi synapse, the depletion model accounts for several features of depression during antidromic spike trains, although it cannot account for the inability to produce depression below 20% despite a fivefold increase in spike frequency (Parker, 1995
Depression at the FETi-FlTi synapse occurs during antidromic spike trains in the absence of presynaptic waveform changes, suggesting that during LR-evoked spike trains several mechanisms combine to produce the observed depression.
Behavioral significance of depression at the FETi-FlTi synapse
The central synaptic connection between FETi and the FlTi motoneurons is thought to be a specialization for the generation of the jumping and kicking motor programs; FETi is usually activated only during kicking or jumping at the same time as the antagonistic FlTi motoneurons are active (Burrows, 1996Depression of the FETi-FlTi synapse may allow FETi activity to contribute to FlTi activity at the onset of co-contraction but enable uncoupling of their activity later in co-contraction, allowing other inputs to determine the pattern of FlTi activity. It may also enable FETi to continue to spike during the period of FlTi motoneuron inhibition that precedes tibial release without exciting the FlTi motoneurons, thus preventing contraction of the FlTi muscle that would reduce the velocity of the tibia once released.
Footnotes
Received Feb. 11, 2003; revised May. 27, 2003; accepted Jun. 13, 2003.This work was supported by a Biotechnology and Biological Sciences Research Council Studentship (J.E.N.) and a Welcome Trust Research Grant (M.B.). We thank H. Robinson, D. Parker, I. Kleppe, and B. Hedwig for discussions and comments on a previous version of this manuscript.
Correspondence should be addressed to Dr. J. E. Niven, Department of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, UK. E-mail: jen22{at}hermes.cam.ac.uk.
Copyright © 2003 Society for Neuroscience 0270-6474/03/237461-09$15.00/0
References
Abbott LF, Sen K, Varela JA, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275: 220-222.
Augustine G (1990) Regulation of neurotransmitter release at the squid giant synapse by presynaptic delayed rectifier current. J Physiol (Lond) 431: 343-364.
[Abstract/Free Full Text] Burns MD, Usherwood PNR (1979) The control of walking in Orthoptera. II. Motor neurone activity in normal free-walking animals. J Exp Biol 79: 69-98.
Burrows M (1995) Motor patterns during kicking movements in the locust. J Comp Physiol [A] 176: 289-305.[Medline]
Burrows M (1996) The neurobiology of an insect brain, p 682. Oxford: Oxford University.
Burrows M, Matheson T (1994) A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor. J Neurosci 14: 272-282.[Abstract]
Burrows M, Watson ADH, Brunn DE (1989) Physiological and ultrastructural characterisation of a central synaptic connection between identified motor neurons in the locust. Eur J Neurosci 1: 111-126.[ISI][Medline]
Cattaert D, El Manira A (1999) Shunting versus inactivation: analysis of presynaptic inhibitory mechanisms in primary afferents of the crayfish. J Neurosci 19: 6079-6089.
[Abstract/Free Full Text] Cattaert D, El Manira A, Clarac F (1992) Direct evidence for presynaptic inhibitory mechanisms in crayfish sensory afferents. J Neurosci 67: 610-624.
Combes D, Meyrand P, Simmers J (1999) Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. J Neurosci 19: 3620-3628.
[Abstract/Free Full Text] Del Castillo J, Katz B (1954) Statistical factors involved in neuromuscular facilitation and depression. J Physiol (Lond) 124: 574-585.
Dunlap K, Fischbach GD (1978) Neurotransmitters decrease the calcium component of sensory neurone action potentials. Nature 276: 837-839.[Medline]
Eccles JC, Katz B, Kuffler SW (1941) Nature of the "endplate potential" in curarized muscle. J Neurophysiol 4: 362-387.
[Free Full Text] Elmqvist D, Quastel DMJ (1965) A quantitive study of end-plate potentials in isolated human muscle. J Physiol (Lond) 178: 505-529.
[Free Full Text] Feng TP (1941) Studies on the neuromuscular junction. Chin J Physiol 16: 341-372.
Finnerty GT, Roberts LSE, Connors BW (1999) Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400: 367-371.[Medline]
Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T (1998) Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20: 797-807.[ISI][Medline]
Gwilliam GF, Burrows M (1980) Electrical characteristics of the membrane of an identified insect motor neurone. J Exp Biol 86: 49-61.
[Abstract/Free Full Text] Heitler WJ, Burrows M (1977) The locust jump. II. Neural circuits of the motor program. J Exp Biol 66: 221-241.
[Abstract/Free Full Text] Hoyle G, Burrows M (1973) Neural mechanisms underlying behaviour in the locust Schistocerca gregaria. I. Physiology of identified motorneurons in the metathoracic ganglion. J Neurobiol 4: 23-41.
Jackson MB, Konnerth A, Augustine G (1991) Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc Natl Acad Sci USA 88: 380-384.
[Abstract/Free Full Text] Klein M, Kandel ER (1980) Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc Natl Acad Sci USA 77: 6912-6916.
[Abstract/Free Full Text] Kusano K, Landau EM (1975) Depression and recovery of transmission at the squid giant synapse. J Neurosci 4: 125-130.
Liley AW, North KAK (1953) An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J Neurophysiol 16: 509-527.
[Free Full Text] Markram H, Wang Y, Tsodyks M (1998) Differential signalling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328.
[Abstract/Free Full Text] Nicholls J, Wallace BG (1978) Modulation of transmission at an inhibitory synapse in the central nervous system of the leech. J Physiol (Lond) 281: 157-170.
[Abstract/Free Full Text] Nusbaum MP, El Manira A, Gossard JP, Rossignol S (1997) Presynaptic mechanisms during rhythmic activity in vertebrates and invertebrates. In: Neurons, networks and motor behavior (Stein PSG, Grillner S, Selverston AI, Stuart DG, eds), pp 237-253. Cambridge, MA: Massachusetts Institute of Technology.
Parker D (1995) Depression of synaptic connections between identified motor neurons in the locust. J Neurophysiol 74: 529-538.
[Abstract/Free Full Text] Parker D (2000) Spinal-cord plasticity. Mol Neurobiol 22: 55-80.[ISI][Medline]
Patil PG, Brody DL, Yue DT (1998) Preferential closed-state inactivation of neuronal calcium channels. Neuron 20: 1027-1038.[ISI][Medline]
Rosenthal J (1969) Post-tetanic potentiation at the neuromuscular junction of the frog. J Physiol (Lond) 203: 121-133.
[Abstract/Free Full Text] Rudomin P, Romo R, Mendell LM (1998) Presynaptic inhibition and neural networks. New York: Oxford UP.
Sabatini BL, Regehr WG (1997) Control of neurotransmitter release by presynaptic waveform at the granule cell to purkinje cell synapse. J Neurosci 17: 3425-3435.
[Abstract/Free Full Text] Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385: 630-634.[Medline]
Sen K, Jorge-Rivera JC, Marder E, Abbott LF (1996) Decoding synapses. J Neurosci 16: 6307-6318.
[Abstract/Free Full Text] Sieglebaum SA, Camardo JS, Kandel ER (1982) Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurons. Nature 299: 413-417.[Medline]
Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 16: 222-226.
Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94: 719-723.
[Abstract/Free Full Text] Usherwood PNR, Grundfest H (1965) Peripheral inhibition of skeletal muscle of insects. J Neurophysiol 28: 497-518.
[Free Full Text] Watson ADH, Burrows M (1981) Input and output synapses on identified motor neurones of a locust revealed by the intracellular injection of horse-radish peroxidase. Cell Tissue Res 215: 325-332.[ISI][Medline]
Wheeler DB, Randall A, Tsien RW (1996) Changes in action potential duration alter reliance of excitatory synaptic transmission on multiple types of Ca2+ channels in rat hippocampus. J Neurosci 14: 5613-5622.
Yawo H, Chuhma N (1993) Preferential inhibition of
-conotoxin-sensitive presynaptic Ca2+ channels by adenosine autoreceptors. Nature 365: 256-258.[Medline]
Zar JH (1996) Biostatistical analysis. Upper Saddle River, NJ: Prentice-Hall, Inc.
Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31. .0[ISI][Medline]
This article has been cited by other articles:
H. Fotowat and F. Gabbiani
Relationship between the Phases of Sensory and Motor Activity during a Looming-Evoked Multistage Escape Behavior
J. Neurosci., September 12, 2007; 27(37): 10047 - 10059.
[Abstract] [Full Text] [PDF]
S. M. Rogers, H. G. Krapp, M. Burrows, and T. Matheson
Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway
J. Neurosci., April 25, 2007; 27(17): 4621 - 4633.
[Abstract] [Full Text] [PDF]
E. G. Antzoulatos and J. H. Byrne
Long-Term Sensitization Training Produces Spike Narrowing in Aplysia Sensory Neurons
J. Neurosci., January 17, 2007; 27(3): 676 - 683.
[Abstract] [Full Text] [PDF]
A. Sakurai, N. R. Darghouth, R. J. Butera, and P. S. Katz
Serotonergic Enhancement of a 4-AP-Sensitive Current Mediates the Synaptic Depression Phase of Spike Timing-Dependent Neuromodulation
J. Neurosci., February 15, 2006; 26(7): 2010 - 2021.
[Abstract] [Full Text] [PDF]
J. E. Niven, M. Vahasoyrinki, M. Juusola, and A. S. French
Interactions Between Light-Induced Currents, Voltage-Gated Currents, and Input Signal Properties in Drosophila Photoreceptors
J Neurophysiol, June 1, 2004; 91(6): 2696 - 2706.
[Abstract] [Full Text] [PDF]
This Article Abstract 
Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science
