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The Journal of Neurophysiology Vol. 79 No. 5 May 1998, pp. 2277-2287
Copyright ©1998 by the American Physiological Society
Department of Physiology and Center for Neuroscience, University of Wisconsin Medical School, Madison,Wisconsin 53706
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Gao, Bao-Xi, Gong Cheng, and Lea Ziskind-Conhaim. Development of spontaneous synaptic transmission in the rat spinal cord. J. Neurophysiol. 79: 2277-2287, 1998. Dorsal root afferents form synaptic connections on motoneurons a few days after motoneuron clustering in the rat lumbar spinal cord, but frequent spontaneous synaptic potentials are detected only after birth. To increase our understanding of the mechanisms underlying the differentiation of synaptic transmission, we examined the developmental changes in properties of spontaneous synaptic transmission at early stages of synapse formation. Spontaneous postsynaptic currents (PSCs) and tetrodotoxin (TTX)-resistant miniature PSCs (mPSCs) were measured in spinal motoneurons of embryonic and postnatal rats using whole cell patch-clamp recordings. Spontaneous PSC frequencies were higher than mPSC frequencies in both embryonic and postnatal motoneurons, suggesting that even at embryonic stages, when action-potential firing rate was low, presynaptic action potentials played an important role in triggering spontaneous PSCs. After birth, the twofold increase in spontaneous PSC frequency was attributed to an increase in action-potential-independent quantal release rather than to a higher rate of action-potential firing. In embryonic motoneurons, the fluctuations in peak amplitude of spontaneous PSCs were normally distributed around single peaks with modal values similar to those of mPSCs. These data indicated that early in synapse differentiation spontaneous PSCs were primarily composed of currents generated by quantal release. After birth, mean mPSC amplitude increased by 50% but mean quantal current amplitude did not change. Synchronous, multiquantal release was apparent in postnatal motoneurons only in high-K+ extracellular solution. Comparison of the properties of miniature excitatory and inhibitory postsynaptic currents (mEPSCs and mIPSCs) demonstrated that mean mEPSC frequency was higher than mIPSC frequency, suggesting that either excitatory synapses outnumbered inhibitory synapses or that the probability of excitatory transmitter release was higher than the release of inhibitory neurotransmitters. The finding that mIPSC duration was several-fold longer than mEPSC duration implied that despite their lower frequency, inhibitory currents could modulate motoneuron synaptic integration by shunting incoming excitatory inputs for prolonged time intervals.
Numerous studies have examined the properties of action potential-independent spontaneous synaptic transmission in the adult mammalian spinal cord (Edwards et al. 1976 Spinal cord preparation
Lumbar spinal cords were isolated from Sprague-Dawley rat embryos at 17-18 days of gestation (E17-18, birth is at E21-22), and from 1- to 3-day-old postnatal rats (P1-3). Pregnant rats were anesthetized lightly and decapitated. Embryos were decapitated quickly, and their spinal cords removed and placed into ice-cold dissecting solution (Ziskind-Conhaim et al. 1993 Whole cell recordings
Whole cell recordings were made from visually identified motoneurons using infrared DIC-videomicroscopy (Dodt and Zieglgansberger 1990 Data analysis
The threshold for synaptic current detection was set at 2 pA above the background noise. Synaptic currents were isolated from the contaminating noise by using both DATAPAC III software (Run Technologies) and visual detection. The same peak detection windows were used for spontaneous PSCs and mPSCs. Examples of histograms of spontaneous PSC and mPSC peak amplitudes and corresponding histograms of peak values of baseline noise are illustrated in Fig. 1. The overlap between these histograms was insignificant therefore, it is unlikely that an appreciable number of small mPSCs were mistakenly regarded as noise events and that mPSC amplitudes were overestimated.
Postnatal increase in the frequency of spontaneous postsynaptic currents
Developmental changes in the frequency of spontaneous PSCs were examined during early stages of synapse formation when a significant increase in the frequency of spontaneous synaptic potentials has been reported (Xie and Ziskind-Conhaim 1995
Developmental changes in the frequency and amplitude fluctuations of mPSCs
To test the hypothesis that the postnatal increases in frequency and amplitude of spontaneous PSCs resulted from an increase in action potential firing in presynaptic pathways, action potentials were blocked by TTX. In the presence of extracellular Mg2+, most TTX-resistant mEPSCs were blocked by CNQX (10 µM), indicating that they were generated by activation of non-NMDA receptors (Cheng et al. 1997
High-K+-evoked mPSCs
The relatively low-frequency spontaneous PSCs at early stages of synapse formation might be indicative of an undifferentiated state of presynaptic membrane components that couple presynaptic depolarization to vesicular transmitter release. To test this possibility, we examined the effects of high-K+-induced depolarization on mPSC frequency and amplitude (Finch et al. 1990
Developmental changes in the properties of mEPSCs and mIPSCs
To determine whether the postnatal increase in mEPSC and mIPSC frequencies was associated with developmental changes in their properties, we compared mPSC peak amplitudes, rise times and decay
Development of synaptic transmission is a fundamental event in the establishment of functional integrated synaptic activity. In this study, we examined the relative roles of presynaptic action potentials and action-potential-independent quantal release in regulating spontaneous synaptic transmission in motoneurons developing in vivo. This study is the first to analyze the properties of excitatory and inhibitory postsynaptic currents simultaneously recorded in motoneurons differentiating in vivo and to determine the relative contribution of excitatory and inhibitory inputs to synaptic integration during early stages of synapse formation.
Mechanisms underlying developmental changes in spontaneous synaptic transmission
Spontaneous PSC frequency is determined by numerous factors, including the firing rate of action potentials invading presynaptic terminals, the number of synaptic inputs on a given neuron, factors that modulate action-potential-independent transmitter release, and receptor activation at the postsynaptic site. Our findings that blocking action potentials reduced spontaneous PSC frequency by ~50% in both embryonic and postnatal motoneurons implied that the functional contribution of presynaptic action potentials to the frequency of spontaneous PSCs did not increase after birth. Therefore the low-frequency spontaneous PSCs in embryonic motoneurons could not be attributed primarily to the low rate of action-potential firing. The finding that action potential contribution to the generation of spontaneous PSCs did not increase after birth was somewhat surprising because of the developmental increase in the frequency of action potential firing along newly established sensorimotor pathways (Fitzgerald 1987 Developmental changes in properties of mEPSCs and mIPSCs
The finding that mEPSC frequency was significantly higher than mIPSC frequency implied that either excitatory synapses outnumbered inhibitory synapses and/or the probability of excitatory transmitter release was higher than the release of inhibitory transmitter. Similar findings have been reported in other studies that examined the nature of newly formed synapses between mammalian neurons developing in vitro (Benson and Cohen 1996
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Lüscher 1990; Redman 1990; Walmsley and Bolton 1994), but little is known about the nature of spontaneous synaptic transmission at early stages of neuronal differentiation in vivo. Studying developmental changes in the properties of action-potential-independent miniature postsynaptic currents (mPSCs) is important for our understanding of the relative roles of pre- and postsynaptic factors in the differentiation of synaptic transmission.
; Xie and Ziskind-Conhaim 1995; Ziskind-Conhaim 1988). The low-frequency spontaneous synaptic potentials recorded in embryonic motoneurons are in sharp contrast to the relatively large, long-lasting dorsal root-evoked synaptic potentials generated in embryonic spinal cords as early as day 15 of gestation (Saito 1979; Ziskind-Conhaim 1990). At that age, the evoked synaptic potentials are produced by excitation of polysynaptic pathways with inputs from excitatory glutamatergic interneurons, and inhibitory glycinergic and GABAergic interneurons (Kudo and Yamada 1985, 1987; Saito 1979; Seebach and Ziskind-Conhaim 1994; Wu et al. 1992). By embryonic day 17-18, primary afferent projections directly synapse onto motoneurons, giving rise to glutamate-mediated monosynaptic potentials. At the same age, descending serotonin-containing axons project into the ventral horn (Ziskind-Conhaim et al. 1993), but their role in modulating synaptic transmission in the immature spinal cord remains largely unknown.
; Gao and Ziskind-Conhaim 1994; Xie and Ziskind-Conhaim 1995; Ziskind-Conhaim 1988), strong inhibitory synapses that transiently dominate synaptic transmission along developing sensorimotor pathways (Nishimaru et al. 1996; Wu et al. 1992), and the undifferentiated state of presynaptic components, which modulate action potential-independent transmitter release.
).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). Postnatal rats were anesthetized by hypothermia. Spinal cord slices were prepared using a procedure described previously (Gao and Ziskind-Conhaim 1995a). Transverse slices (350 µm) were cut using a Vibrotome. Slices were transferred into a recording chamber and held on the glass-bottom chamber with a grid of nylon threads. The submerged slices were perfused with extracellular solution gassed with 95% O2-5% CO2 and maintained at room temperature (21-23°C). The extracellular solution contained (in mM) 113 NaCl, 3 KCl, 2 CaCl2, 1 MgCl2, 25 NaHCO3, 1 NaH2PO4, and 11 glucose (pH 7.2).
2-amino-5-phosphonovaleric acid (D-APV), 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), strychnine, and bicuculline methchloride from Research Biochemicals.
; MacVicar 1984). The largest multipolar or round cells (15-25 µm diam) in the lateral and medial ventral horn were identified as motoneurons (Gao and Ziskind-Conhaim 1995a; Takahashi 1978). Patch pipettes with a tip diameter of 2-3 µm and DC resistance of 4-8 M
were fabricated using a Flaming-Brown P-97 puller (Sutter Instruments). The pipette solution contained (in mM) 140 Cs-gluconate, 9 CsCl, 1 Mg-ATP, 0.1 GTP, 10 N-2-hydroxyethylpiperazine-N'2-ethanesulfonic acid, and 0.2ethylene glycol-bis(
-aminoethyl ether)-N,N,N',N'-tetraacetic acid(buffered to pH 7.2 with CsOH). After the formation of a giga seal and breaking through the membrane, the cell capacitance was compensated by adjusting the compensation dial. The series resistance was 8-15 M, and it was compensated >60%. To record both excitatory and inhibitory synaptic currents, experiments were performed at a holding membrane potential of 40 mV. All recordings were corrected for the liquid junction potential (13 mV) (Gao and Ziskind-Conhaim 1995a).
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FIG. 1.
Histograms of peak amplitudes of spontaneous excitatory postsynaptic currents (sEPSCs), miniature EPSCs (mEPSCs), and events detected in the baseline noise in recordings carried out in a postnatal day 1 (P1) motoneuron. Fluctuations in peak amplitude of inward synaptic currents were compared with the fluctuations in downward deflections in the baseline noise. Therefore mostly positive values were presented in amplitude histograms of noise events. Similarly, for inhibitory postsynaptic current (IPSC) measurements, only upward deflections in the noise baseline were analyzed (not shown). Before tetrodotoxin (TTX) application, the mean amplitude of noise events ( 
) was 2.1 pA. Histogram of sEPSC peak amplitudes was skewed (
) and could not be fitted by a Gaussian curve. In the presence of TTX, mEPSC peak amplitudes were normally distributed () with a mean of 5.8 pA. Histogram of the corresponding noise events () had a mean amplitude of 2.1 pA. Recordings of sEPSCs (n = 356) and mEPSCs (n = 151) were carried out for 5 min. Binwidth is 1 pA for this and all other figures.
3 ms were included in amplitude analyses. The cutoff for inhibitory currents was 5 ms. The cutoff criteria for inclusion of currents were based on preliminary data demonstrating that the rising times for large miniature excitatory PSC (mEPSCs; 
10 pA) varied between0.3 and 3 ms, whereas those for large miniature inhibitory PSCs (mIPSCs) varied between 0.3 and 5 ms. There was no correlation between the amplitude and rise time of those currents, indicating that they were not affected by cable attenuation.
5 bins (Edwards et al. 1990). However, amplitude histograms constructed with binwidths of 2-3 pA were not significantly different from those based on binwidths of 1 pA (see also Edwards et al. 1990).
), and duration. mPSC decays were best fitted with single exponential curves that were superimposed on mPSCs. mPSC duration was measured as the time from 10% of peak current to 90% return to baseline. Analyses of mPSC properties included all currents with monotonic rise and decay phases, regardless of the rise time. Data are presented as means ± SE. Student's t-test was used to determine the statistical significance of the results. The level of statistical significance was 5%.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
; Ziskind-Conhaim 1988). Currents wererecorded at E17-18 and P1-3. To distinguish between excitatory and inhibitory currents, motoneurons were held at a membrane potential of 40 mV (Fig. 2A). The reversal potential for both glycine- and 
-aminobutyric acid (GABA)-mediated inhibitory currents is 66 mV (Gao and Ziskind-Conhaim 1995a). The inward currents were blocked by D-APV (20 µM) and CNQX (10 µM; Fig. 2B), antagonists of N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor subtypes, indicating that they were glutamate-mediated excitatory synaptic currents. The outward currents were eliminated by strychnine (5 µM) and bicuculline (20 µM, Fig. 2B), suggesting that they were generated by activation of glycine- and GABAA-gated receptors.
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FIG. 2.
A: amplitude fluctuations in spontaneous PSCs recorded in embryonic day 17 (E17) and P2 motoneurons. Simultaneous recordings of spontaneous inward and outward postsynaptic currents at a holding membrane potential of 40 mV. Spontaneous EPSCs (inward currents) and IPSCs (outward currents) were recorded continuously at P2 but only a sample of traces with PSCs are illustrated at E17. At E17, sEPSC and sIPSC frequencies were 0.48 and 0.16 Hz, respectively, and at P2 they were 0.79 and 0.63 Hz. B: spontaneous EPSCs and IPSCs recorded continuously in a P1 motoneuron. Inward sEPSCs (control) were blocked by 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 µM) and D2-amino-5-phosphonovaleric acid (D-APV, 20 µM), and outward sIPSCs were blocked by bicuculline (20 µM) and strychnine (5 µM). Holding membrane potential was 40 mV.
; Ziskind-Conhaim 1988). It is likely that the higher signal-to-noise ratio of the whole cell recording technique provided a better resolution for detecting smaller synaptic events than those recorded using intracellular microelectrodes.
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TABLE 1.
Frequencies of spontaneous PSCs and mPSCs increased after birth
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FIG. 4.
Histograms of sIPSC and mIPSC peak amplitudes recorded in E17 and P1 motoneurons. At E17, sIPSC and mIPSC peak amplitudes were normally distributed and were fitted by single Gaussian curves (smooth curves) with means at 6.6 and 6.1 pA, respectively. At P1, the histogram of sIPSC peak amplitudes could not be fitted by Gaussian distribution, but a single Gaussian curve fitted mIPSC amplitude distribution with a mean of 5.6 pA. At E17, sIPSC and mIPSC frequencies were 0.20 and 0.15 Hz, respectively and they increased to 0.54 and 0.18 Hz, respectively, after birth. Number in brackets are the number of PSCs included in each amplitude histogram.
). The outward currents were blocked partially by either strychnine (5 µM) or bicuculline (20 µM), suggesting that mIPSCs were composed of both glycine and GABAA receptor-mediated currents (Gao et al. 1997).
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FIG. 3.
Amplitude histograms of sEPSCs and TTX-resistant mEPSCs recorded in E17 and P2 motoneurons. Fluctuations in sEPSC and mEPSC peak amplitudes were normally distributed and were well fitted by single Gaussian curves (smooth curves). Based on Gaussian curves, at E17 mean sEPSC and mEPSC amplitudes were 6.2 and 5.9 pA, respectively, and at P2 their means were 13.3 and 7.3 pA, respectively. At E17, sEPSC and mEPSC frequencies were 0.37 and 0.26 Hz, respectively, and higher frequencies of 1.0 and 0.44 Hz, respectively, were recorded after birth. Number in brackets are the number of PSCs included in each histogram.
).
; Gottmann et al. 1994; Liu and Tsien 1995). Various extracellular K+ concentrations were examined (10-32 mM), and 18 mM appeared to be the optimal concentration for increasing mPSC frequency without causing a significant overlap of synaptic currents (Fig. 5, 
). Overlapping currents were excluded from analyses of amplitude distributions.
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FIG. 5.
Frequency of high-K+-evoked mPSC was significantly higher than mPSC frequency in an E17 motoneuron. A: mEPSCs and mIPSCs were recorded continuously before (TTX) and after application of 18 mM extracellular K+ (TTX + high-K+). High-K+-evoked increased frequency was occasionally associated with overlapping currents ( ), but those were not included in data analyses. Occasionally, recordings became noisier in the presence of high-K+ solution probably as the result of activation of voltage-dependent Ca2+ channels. B: amplitude histograms of mPSC peak amplitudes recorded in the same motoneuron illustrated in A. In TTX-containing solution, mEPSC and mIPSC unimodal amplitude distributions were fitted with single Gaussian curves (smooth curves) with means at 5.2 and 4.4 pA, respectively. Frequencies of mEPSCs and mIPSCs were 0.20 and 0.09 Hz, respectively, and increased to 0.50 and 0.29 Hz, respectively, in high-K+ solution. The two- to threefold increase in high-K+-evoked mPSC frequencies was correlated with larger mPSCs. Amplitude histogram of high-K+-evoked mEPSCs was skewed toward large currents and could not be fitted by normal Gaussian distribution. Amplitude distribution of high-K+-evoked mIPSCs was fitted with a single Gaussian curve with a mean at 6.2 pA. Number in brackets are the number of mPSCs included in each histogram.
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FIG. 6.
mPSC frequency and amplitude in a P2 motoneuron significantly increased in high-K+ extracellular solution. A: mEPSCs and mIPSCs were recorded continuously before (TTX) and after application of 18 mM extracellular K+ (TTX + high-K+). B: amplitude histograms of the currents recorded in the same motoneuron illustrated in A. Frequencies of high-K+-evoked mEPSCs and mIPSCs were two- to threefold higher than those recorded in the presence of TTX alone. At P2, mEPSC and high-K+-evoked mEPSC frequencies were 0.30 and 0.75 Hz, respectively, and mIPSC and high-K+-evoked mIPSC frequencies were 0.18 and 0.55 Hz, respectively. Higher frequencies were correlated with larger mPSC amplitudes as evident by the change from a single Gaussian curve (TTX, smooth curve) to a sum of 2-3 Gaussian curves (TTX + high-K+). Based on Gaussian curves, mean amplitude of mEPSCs (TTX) was 5.5 pA, and the multiple peaks in amplitude distribution of high-K+-evoked mEPSCs corresponded to means of 5.4, 9.7, and 16.7 pA. Mean mIPSC amplitude (TTX) was 5.6 pA, and the means of the 2-peak amplitude distribution of high-K+-evoked mIPSCs were 5.6 and 11.0 pA. Number in brackets are the number of mPSCs in each histogram.
s at E17-18 and P1-3 (Table 2). In the presence of extracellular Mg2+, the majority of mEPSCs were non-NMDA receptor-mediated currents (Cheng et al. 1997). Infrequently (<0.01 Hz), slow-rise, long-duration NMDA receptor-mediated mEPSCs were recorded, but those were excluded from data analyses. mIPSCs were comprised of both glycine- and GABA-mediated currents, but because of their similar properties (Gao et al. 1997), both mIPSC populations were pooled for quantitative analyses.
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TABLE 2.
Developmental changes in basic kinetic properties of mEPSCs and mIPSCs
significantly increased from 2.2 ms at E17 to ~4.0 ms at P1-3 (Table 2). However, the developmental changes in mIPSC decay s were not significant, and values of 24.0 and 15.8 ms were measured in embryonic and postnatal motoneurons, respectively.
was at least fourfold shorter than mIPSC rise time and decay . The slower rise time and longer decay of mIPSCs resulted in significantly longer duration mIPSCs than mEPSCs. At E17, mean mIPSC and mEPSC durations were 45.9 and 7.8 ms, respectively. Smaller but significant difference between mIPSC and mEPSC durations persisted after birth, when their mean durations were 46.3 and 23.3 ms, respectively.
; Ulrich and Lüscher 1993; reviewed by Redman 1990).
s and rise times were examined (Fig. 7). Correlation between these parameters within a given neuron would indicate that cable attenuation introduced a significant distortion in mIPSC properties (Rall 1969). The lack of correlation between these parameters in all motoneurons studied (n = 9) suggested that mIPSC slow kinetics resulted from intrinsic properties of glycine and GABA receptors rather than distortion due to dendritic filtering. Similarly, there was no correlation between mEPSC amplitudes and rise times and between their decay s and rise times (not shown). We cannot rule out the possibility that the lack of correlation between these properties might be indicative of larger intrinsic variability than the variability expected from electrotonic locations.
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FIG. 7.
Lack of correlation between basic kinetic properties of mIPSCs in a P1 motoneuron. mIPSC peak amplitudes were plotted against their rise times, and their decay s were plotted against their rise times. In both cases, there was no correlation between these parameters (r = 0.004-0.36).
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Our data suggested that the twofold postnatal increase in mPSC frequency resulted from either an increase in the number of synaptic inputs converging onto motoneurons or an enhanced probability of transmitter release.
), but it significantly reduces the frequency of both small and large spontaneous potentials in motoneurons developing in organotypic spinal cord slices (Streit and Lüscher 1992).
; Gottmann et al. 1994; Jackson et al. 1982). Several studies have suggested that early in spinal cord differentiation, inhibitory synapses transiently dominant synaptic transmission along sensorimotor pathways (Nishimaru et al. 1996; Wu et al. 1992). However, based on our data, it is unlikely that such predominant inhibitory synapses were formed directly on motoneurons.
suggested that dendritic filtration did not introduce a major error in mPSC shape and size. Similarly, it has been suggested that the variability in mPSC amplitude and shape in developing neurons in the hippocampus and neocortex is not attributed to cable attenuation (Burgard and Hablitz 1993; McBain and Dingledine 1992). Moreover, large variability in mPSC amplitudes was apparent in neurons that lack dendrites (Callister and Walmsley 1996). In bushy cells of the anteroventral cochlear nucleus, the substantial variability in mPSC sizes was attributed to intrinsic fluctuations in quantal release and in the number of receptors at each release site (Isaacson and Walmsley 1996). Current fluctuations could arise from a number of other factors including the time course of diffusion and uptake of the transmitter and receptor affinity (Kitzing et al. 1994).
; Kraszewski and Grantyn 1992).
). In other neurons differentiating in culture, it has been shown that quantal release activates only a small fraction of receptors. For example, only a fraction of glutamate receptors clustered opposite release sites contributes to mEPSCs in differentiating motoneurons (Vogt et al. 1995). Similarly, it has been suggested that in dissociated spinal neurons differentiating in vitro, activation of only 10 NMDA channels is required for generating a 20 pA mEPSC (Ascher et al. 1988), and openings of only a few GABAA receptors are necessary for the production of mIPSCs (Edwards et al. 1990).
increased almost twofold. Therefore, it is conceivable that channel kinetics and/or factors involved in transmitter uptake changed immediately after birth. It is unknown whether additional changes in mEPSC properties occur at later stages of spinal cord maturation, but the time course of mEPSCs in postnatal motoneurons is within the range of values reported for primary afferent-evoked excitatory postsynaptic potentials in spinal cords of adult cats (Redman and Walmsley 1983).
did not change during the period studied. mIPSC mean decay was 15.9 ms in postnatal motoneurons, similar to the decay of evoked IPSCs recorded in sensory spinal neurons of newborn rats (17.8 ms) (Takahashi et al. 1992). In those neurons, the decrease in decay s occurs only 2-3 wk after birth.
). The relative slow rise and decay times of mIPSCs compared with those of mEPSCs are probably indicative of differences in receptor gating kinetics rather than their generation at distal synaptic sites. Moreover, substantial electrophysiological and morphological evidence indicates that in mammalian spinal cords, inhibitory synapses concentrate on motoneuron somata and proximal dendrites (Burke et al. 1971; Örnung et al. 1996).
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ACKNOWLEDGEMENTS |
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We thank Drs. Peter Lipton, Meyer Jackson, and Robert Conhaim for critical comments on the manuscript.
This work was supported by the National Institute of Neurological Disorders and Stroke Grant NS-23808 to L. Ziskind-Conhaim.
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FOOTNOTES |
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Address for reprint requests: L. Ziskind-Conhaim, Dept. of Physiology, 129 SMI, University of Wisconsin Medical School, 1300 University Ave., Madison, WI 53706.
Received 14 November 1997; accepted in final form 9 February 1998.
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Abstract
Introduction
Methods
Results
Discussion
References
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D. W. Ali, R. R. Buss, and P. Drapeau Properties of Miniature Glutamatergic EPSCs in Neurons of the Locomotor Regions of the Developing Zebrafish J Neurophysiol, January 1, 2000; 83(1): 181 - 191. [Abstract] [Full Text] [PDF]
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J. Rohrbough and N. C. Spitzer Ca2+-Permeable AMPA Receptors and Spontaneous Presynaptic Transmitter Release at Developing Excitatory Spinal Synapses J. Neurosci., October 1, 1999; 19(19): 8528 - 8541. [Abstract] [Full Text] [PDF]
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S. Oleskevich, F. J. Alvarez, and B. Walmsley Glycinergic Miniature Synaptic Currents and Receptor Cluster Sizes Differ Between Spinal Cord Interneurons J Neurophysiol, July 1, 1999; 82(1): 312 - 319. [Abstract] [Full Text] [PDF]
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B.-X. Gao and L. Ziskind-Conhaim Development of Ionic Currents Underlying Changes in Action Potential Waveforms in Rat Spinal Motoneurons J Neurophysiol, December 1, 1998; 80(6): 3047 - 3061. [Abstract] [Full Text] [PDF]
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