Departments of Physiology and , 1 Morphological Science, Faculty of Medicine, Kyoto University, Kyoto 606, Japan
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Abstract |
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Introduction |
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In the present study, it was found that a group of RS neurons could generate bursts of attenuated spikes, presumably through activation of recurrent axon collaterals of PT cells. The burst was triggered from the long-lasting depolarization which appeared to be distinct from EPSPs. These RS neurons were multipolar in shape, and had sparsely spiny dendrites and numerous horizontally spreading axonal networks, suggesting that they are inhibitory interneurons. It is hypothesized that this group of RS neurons may be involved in inducing recurrent IPSPs in PT cells.
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Materials and Methods |
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The methods are basically similar to those described in previous studies (Kang et al., 1988, 1991
). The experiments were carried out on cats weighing between 3.0 and 5.0 kg. The cats were anesthetized with pentobarbital (35 mg/kg, i.p.) and the trachea and a superficial vein of the distal forelimb were cannulated. The animals were mounted on a stereotaxic instrument and immobilized with pancuronium bromide (0.05 mg/kg/h, i.m.) after artificial ventilation. Additional doses of pentobarbital (1.5 mg/kg/h, i.v.) were given to maintain anesthesia. Body temperature was maintained between 36 and 38°C by a heating pad. A craniotomy was performed over the left motor cortex. The cortical surface was perfused with normal Ringer solution maintained at 36°C. Three pairs of bipolar stimulating electrodes (diameter 0.2 mm, interpolar distance 1 mm), whose tips were set at three different ventrodorsal levels separated by 1 mm, were placed stereotaxically in the medullary pyramid and in the more dorsal structures (the trapezoid body and the lemniscus medialis). Two similar pairs of bipolar stimulating electrodes were also placed stereotaxically in the ventrolateral (VL) nucleus of the thalamus (A, 1011; L, 35; H, 12). Stimulation (0.2 ms duration, intensity
1.0 mA) was applied through these bipolar electrodes. Using a small silver-ball electrode, the electroencephalogram was monitored monopolarly at the dimple of the sensorimotor cortex to assess the general level of anesthesia and to adjust the final position of the stimulating electrode at the pyramid to produce
and ß waves (Jabbur and Towe, 1961
; Takahashi, 1965
). The location of the stimulating electrodes was also histologically verified by making lesions after recording. Two types of glass microelectrodes filled with 2 M potassium citrate (DC resistances, 510 and 2040 M
respectively) were used to obtain extracellular and intracellular recordings from the lateral part of the cruciate sulcus (area 4
). The input signal was fed into a high-input impedance DC preamplifier (MEZ-8201, Nihon Kohden) which was connected to an AC amplifier of the oscilloscope (VC-8 and 9, Nihon Kohden) with a time constant of 0.1 s. Responses were photographed directly from the screen of the oscilloscope. In the present in vivo study, extracellular and intracellular recordings were selected from a large number of recordings which were made in this laboratory from 1969 to 1986, in order to collect samples of rare neurons. In in vivo experiments, intracellular staining was not practical for such rare neurons.
In Vitro Slice Experiments
The experimental procedure was the same as that in the previous studies (Kang and Kayano, 1994; Kang et al., 1994
). Cats weighing 3.04.0 kg were anesthetized with pentobarbital sodium (35 mg/kg, i.p.). They were positioned in a stereotaxic frame. After a craniotomy over the left motor cortex, the animal was killed by overdose injection of pentobarbital. The lateral part of the cruciate sulcus (area 4
) was quickly excised with a razor blade. With a vibratome, parasagittal slices of 500 µm thickness were cut from the lateral end of the cruciate sulcus medially up to 3 mm. Slices were preincubated in oxygenated Krebs solution at room temperature for ~110 h before recording. Slices were then transferred into a recording chamber of the interface type. The temperature of the chamber was maintained at 35°C.
Under the dissecting microscope, the borderline between the gray and the white matter of the motor cortex was easily discernible. Usually, the recording electrode was positioned at a site slightly above the border line. All the cells thus recorded were found to be located in either layer V or VI when they were able to be histologically recovered.
The Krebs solution (pH 7.4) was composed of (in mM): NaCl 124, KCl 3.5, KH2PO4 1.25, NaHCO3 26, CaCl2 2.4, MgSO4 1.3, and glucose 10. Glass pipettes filled with 13% biocytin in 0.05 M TrisHCl and either 0.5 M KCl or 1 M potassium methylsulfate (pH 7.07.4) were used for recording. The DC resistance of the recording electrodes was between 70 and 150 M. The input signal was fed into a high-input impedance DC amplifier with an active bridge circuit (IR-183, Neurodata), which was connected to a digital oscilloscope (VC-11, Nihon Kohden) and stored on a four-channel FM tape recorder (DFR-3515, Sony). Microstimulation (0.2 ms duration, 110 µA) was applied at a site 200500 µm horizontally remote from the recorded cell body in layer VI or at white matter (WM) through a tungsten microelectrode (impedance 0.51.0 M
at 5 kHz) which was usually positioned at a depth of 200300 µm from the surface of slices. Data were plotted either on an XY plotter (MP 100001, Watanabe) or through a laser printer (HP-4LJpro). All values given in the text are expressed as mean ± SD. Statistical significance was examined using two-tailed t-test. Histological procedures were the same as those in the previous study (Kang and Kayano, 1994
; Kang et al., 1994
).
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Results |
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In in vivo experiments, extracellular and intracellular record- ings were obtained from cortical neurons in area 4 of the cat motor cortex. In extracellular recordings, there were non- pyramidal tract (non-PT) neurons that displayed bursts of 1020 spikes in response to stimulation of either pyramid or VL nucleus. It should be noted that non-PT neurons are not neces- sarily equivalent to non-pyramidal shaped neurons. As seen in Figure 1Aa,
a burst of five spikes was induced in a non-PT neuron following pyramid stimulation. With an increase in the stimulus intensity, the number of spikes during bursts increased almost linearly (Fig. 1Ab
). However, the latency to the first spike of the burst varied in response to stimulation even with the same intensity and did not necessarily decrease with an increase in the stimulus intensity (compare Fig. 1Aa and Ab
). This indicates that these spikes were evoked orthodromically (trans-synaptically) but not antidromically, and therefore the neuron was identified as a non-PT neuron. VL stimulation with a maximum intensity (1 mA) induced only one spike in this non-PT neuron (Fig. 1Ac
). In contrast, VL stimulation evoked bursts of spikes in another non-PT neuron as shown in Figure 1Ba
. However, in this non-PT neuron, pyramid stimulation evoked only one spike (Fig. 1Bc
). Thus, there appeared to be two separate groups of burst non-PT neurons which were activated predominantly or almost exclusively by VL and pyramid stimulation respectively. This categorization of burst neurons based on the dependence on inputs was further confirmed by differences in the spiking nature between the two subtypes of burst neurons.
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In some of the burst non-PT neurons, both pyramid and VL stimulation triggered bursts. Depending on the ratio of the maximum spike number triggered by VL stimulation to that by pyramid stimulation, burst non-PT neurons were separated into either VL-dependent (ratio >1) or pyramid-dependent (ratio <1) burst neurons. The maximum degree of reduction of spike amplitude during bursts was significantly larger (P < 0.01) in pyramid-dependent burst neurons (38.9 ± 9.7%, n = 12) than in VL-dependent burst ones (11.0 ± 3.6%, n = 11). Thus, pyramid- and VL-dependent burst neurons displayed attenuated and less-attenuated spikes respectively during bursts. Accordingly, burst non-PT neurons were also classified into the two subtypes based on the degree of spike attenuation being >25% or <20%. All 11 pyramid-dependent burst neurons were classified as those bursting with attenuated spikes (filled circles in Fig. 2A) while 11 out of 12 VL-dependent burst neurons were those bursting with less-attenuated spikes (open circles in Fig. 2A
). Pyramid- dependent burst neurons tended to be located in deeper layers than VL-dependent burst neurons, as illustrated in Figure 2A
. The mean depth from the cortical surface where VL-dependent burst neurons were encountered was 0.92 ± 0.38 mm (n = 11) and that for pyramid-dependent burst neurons was 1.27 ± 0.28 mm (n = 12). This difference in the depth of location was significant (P < 0.05).
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In Vivo Intracellular Recordings
Over 200 cortical neurons were intracellularly recorded in deep cortical layers whose depth from the cortical surface ranged from 1.0 to 1.8 mm. Among these neurons were 73 non-PT neurons in which pyramid stimulation did not induce anti- dromic spikes. Of these 73 neurons, six and three neurons displayed bursts of spikes in response to stimulation of pyramid and VL respectively. The mean depths where these six and three neurons were encountered were 1.32 ± 0.29 and 1.30 ± 0.31 mm respectively. Although there was no significant difference (P > 0.05) in the mean depth between neurons displaying pyramid- and VL-dependent bursts, the incidence of impalement in deep cortical layers appeared to be higher in neurons displaying pyramid-dependent bursts.
Intracellular recordings revealed that a burst of variably attenuated spikes evoked by pyramid stimulation was triggered from a prolonged depolarization. As shown in Figure 3Aa, bursts of attenuated spikes with frequency adaptation were induced in a non-PT neuron by pyramid stimulation. In the same non-PT neuron, prominent EPSPs were evoked by a subthreshold pyramid stimulation (Fig. 3Ab
), whereas a strong VL stimulation evoked only small EPSPs and failed to induce spikes (Fig. 3Ac
). These bursts of attenuated spikes of varying amplitudes usually deteriorated rapidly in response to repetitive pyramid stimu- lation, leaving only the first spike almost unchanged. In another non-PT neuron, pyramid stimulation induced a single spike followed by either a train of small spike-like potentials occurring at 360500 Hz or a long-lasting depolarization alone (Fig. 3Ba
), while VL stimulation evoked no apparent EPSPs. Since the train of small spike-like potentials was evoked in an all-or-nothing manner, these potentials could be considered as abortive or attenuated spike potentials. Such a train of small spike potentials also tended to deteriorate and disappear after occurring several times in response to repetitive pyramid stimulation. Thereafter, in the same non-PT neuron, the same pyramid stimulation no longer induced such a train of small spike potentials, but induced only the first spike followed by a long-lasting depolari- zation (Fig. 3Bb
). In six non-PT neurons which displayed pyramid-dependent bursts of attenuated spikes, the duration at half amplitude of the first spike was 0.94 ± 0.32 ms (n = 6), and subthreshold pyramid stimulation (<0.5 mA) evoked prominent EPSPs at latencies of 2.4 ± 0.5 ms (n = 6) while strong VL stimulation (0.51.0 mA) evoked small EPSPs at latencies of 3.0 ± 2.2 ms (n = 4), hardly triggering bursts. Thus, in deep cortical layers of the cat motor cortex, there was a group of non-PT neurons in which a characteristic burst of attenuated spikes emerging from the long-lasting depolarization was seen in response to pyramid stimulation. By contrast, as has been reported previously (Kang et al., 1988
, 1991
; Ghosh and Porter, 1988
), pyramid stimulation never triggered bursts in PT cells.
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In Vitro Intracellular Recording
In order to further elucidate the electrophysiological and morphological properties of burst non-PT neurons located in deep cortical layers, intracellular recordings were made from layers V and VI cortical neurons in in vitro slice preparations, and biocytin was intracellularly injected. Stable intracellular recordings could be obtained from 75 layer V and VI neurons, and 67 of these were recovered morphologically; 42 and 25 of them were identified to be pyramidal and non-pyramidal cells respectively. Either WM or layer VI was stimulated to find neurons that display either a burst of attenuated spikes with frequency adaptation or a spike followed by a long-lasting after-depolarization, similar to that seen in pyramid-dependent burst neurons in in vivo experiments.
An involvement of N-methyl-D-aspartate (NMDA) responses in the generation of burst firing has been reported (Hoffman and Haberly, 1989; Kobayashi et al., 1993
). As shown in Figure 4AC
, layer V and VI pyramidal cells (n = 5 and 6 cells respectively) usually display NMDA EPSPs in response to stimulation of deep layers (V/VI), and the removal of voltage-dependent Mg2+ block of NMDA receptors by membrane depolarization leads to a generation of bursts (n = 3). However, since pentobarbital partially suppresses NMDA responses indirectly (Pennartz et al., 1990; Kanter et al., 1996
) presumably through an enhancement of GABAA responses (Malherbe, 1990; Sigel et al., 1990
) or directly (Daniell, 1994
), the activation of NMDA receptors are not likely to be largely involved in the generation of pyramid-dependent bursts in non-PT neurons recorded under pentobarbital anesthesia. Therefore, in order to discriminate the NMDA-dependent burst from those seen under the anesthetized condition, in vitro slice experiments were conducted in the presence of APV (50 µM).
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As shown in Figure 6A, with an increase in the intensity of WM stimulation (46 µA), EPSPs which were evoked in a layer VI RS non-pyramidal cell in the presence of APV (50 µM) increased in amplitude (open circles in Fig. 6C
) but only slightly increased in half-duration (open square in Fig. 6C
). After triggering a spike with a stronger stimulation (7 µA), however, the decay time- course of the after-depolarization following the spike became slower than those of EPSPs (see inset in Fig. 6A
). A further increase in the stimulus intensity to 9 µA led to generation of a burst of three attenuated spikes followed by another after- depolarization with a further slower decay time course (Fig. 6A
, top trace). By applying stimulation with the same intensity (9 µA) as triggered the burst of three spikes (top trace in Fig. 6A
), a burst of five attenuated spikes with frequency adaptation could also be induced (Fig. 6B
). Thus, even in response to stimulation with a constant intensity (9 µA; Fig. 6C
), the number of spikes in the bursts varied from two to five, and the half-duration of the long-lasting depolarization underlying the burst changed from 43 to 83 ms (filled squares, Fig. 6C
) in association with the spike number. The half-duration was closely correlated with the spike number (r = 0.98) (Fig. 6D
, open circles). Thus, the half-duration of the long-lasting depolarization and the number of spikes during bursts concurrently and strongly fluctuated in response to stimulation with a constant intensity even in the presence of APV that might suppress polysynaptic action.
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We also encountered seven neurons that displayed fast repetitive firing (>150 Hz) without marked frequency adaptation in response to an injection of depolarizing current pulses. VL- dependent burst non-PT neurons seen in in vivo experiments may correspond to FS neurons, because high-frequency burst firings could be induced without prominent frequency adap- tation in both types of neurons. As seen in Figure 9Aa,b, a sharp action potential was followed by a large and fast AHP and a train of fast repetitive firing was induced in a non-pyramidal cell by injections of depolarizing current pulses. Similarly, four of the seven neurons displayed a sharp action potential with a duration at half-amplitude of 0.44 ± 0.03 ms, followed by a large and fast AHP whose amplitude and duration ranged 13 to 20 mV and 12 to 20 ms respectively. Based on these parameters of action potentials and fast repetitive firing pattern as reported previously (McCormick et al., 1985
; Kawaguchi, 1993
), these four neurons were regarded as FS neurons. In the four neurons, the resting membrane potential and the input resistance were 59.6 ± 3.8 mV and 40.1 ± 5.7 M
respectively, and the spike amplitude was 72.8 ± 6.5 mV. The remaining three neurons displayed somewhat different characteristics of spikes; the spike half-duration (0.580.90 ms) was appreciably longer than that in FS neurons and the amplitude of AHP (510 mV) was smaller than that in FS neurons, and the duration of AHP (46 ms) was also shorter than that in FS neurons (cf. Fig. 9A
with Fig. 9B
). Therefore, these neurons were separately categorized as FS-like neurons. Neither bursts nor the long-lasting depolarization was observed in these seven FS and FS-like neurons in response to stimulation of WM or deep layers in the presence of APV. This suggests that NMDA receptors play an important role in generating bursts in FS neurons, as has been suggested previously (Jones and Buhl, 1993
; Kawaguchi, 1993
).
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Discussion |
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Extracellular versus Intracellular Recordings
Using an extracellular recording method in in vivo experiments, we have identified the two types of burst neurons: VL-dependent and pyramid-dependent burst non-PT neurons. The spike amplitude attenuation and spike frequency adaptation were more prominent in pyramid-dependent burst non-PT neurons than in VL-dependent burst non-PT neurons. On the other hand, in in vivo intracellular recordings, similar input-specific bursts were induced in the two distinct types of non-PT neurons though their numbers were small. The identification of the same neuron types in in vivo extracellular and intracellular recordings was based on the following three criteria: (i) the input specificity (VL versus pyramid stimulation); (ii) the presence or absence of the marked attenuation of spike amplitude during bursts; and (iii) the presence or absence of prominent frequency adaptation during bursts. There was only one burst neuron displaying bursts of attenuated spikes among 12 VL-dependent burst neurons, and all 11 pyramid-dependent burst neurons displayed bursts of attenuated spikes (Fig. 2A). Therefore, it is likely that the intracellularly recorded spike activities of FS neurons and burst neurons with attenuated spikes emerging from the long-lasting depolarization are reflected in the extracellular recordings of VL-dependent and pyramid-dependent burst non-PT neurons respectively.
As to the correspondence of burst neurons with attenuated spikes emerging from the long-lasting depolarization between the in vivo and the in vitro intracellular recordings, the input specificity among the three criteria could not be examined in in vitro slice preparations. However, those burst neurons were invariably located in deep layers of the cat motor cortex both in in vivo and in vitro preparations. The characteristic long-lasting depolarization, from which a train of attenuated spikes emerged in a pattern with frequency adaptation, was commonly observed in in vivo and in in vitro preparations. Therefore, these burst neurons obtained in in vitro intracellular recordings were presumed to be the same type of neurons as pyramid-dependent burst neurons in in vivo experiments.
Non-synaptic Nature of Long-lasting Depolarization in Presumed Pyramid-dependent Burst Neurons
The peak level of the long-lasting depolarization was not affected by varying baseline membrane or holding potentials (Fig. 7). With membrane hyperpolarization, the peak level of EPSPs (Vmp) usually shifts towards the same direction as that of the shift of the holding potential (Vh), as observed previously (Coombs et al., 1955a
,b
) and should be somewhere in between Vh and the reversal potential (Erev) (see Appendix). Regardless of Vh, Vmp can remain constant at Erev only when the shunting resistance at subsynaptic membrane (RS) is 0. In such a case (RS = 0), the amplitude of EPSPs is as large as the driving potential, and the slope of the line representing the linear relation between Vh and EPSPs amplitudes is 1. However, RS cannot be zero in any type of synapse, and the Erev of most EPSPs is usually ~0 mV (Kuffler et al., 1984
). Thus, the constant peak level and the hyper- polarized reversal potential would indicate the non-synaptic nature of the long-lasting depolarization.
However, it is possible that some outward currents may have prevented Vmp from reaching a more depolarized value and kept Vmp constant, and consequently the linear extrapolation of plottings of such apparent amplitudes of EPSPs against Vh may have resulted in an unusually hyperpolarized Erev (Fig. 7A, continuous line). As described in the Appendix, the slope of a straight line representing a linear relation between the amplitude of EPSPs and Vh must be between 1 and 0 (Fig. 7A
, interrupted line) unless outward currents affect Vmp. If the present results were due to some outward currents, the outward currents should have increased with depolarization of Vh to make the slope as steep as 1 and to make the straight line intersect the X-axis at a Vh much more hyperpolarized than 0 mV (Fig. 7A
, continuous line). However, because of the voltage- dependent inactivation, the activation of transiently inactivating outward currents should be decreased with depolarization of Vh from 102 to 60 mV, contrary to what was presumed. Involvements of non-inactivating outward currents may also be unlikely because of their activation threshold (>40 mV). Taken together, it is unlikely that the Erev was shifted to an unusually hyperpolarized membrane potential and was kept at a constant level due to these outward currents.
Dendritic Calcium Spike versus Long-lasting Depolarization
The long-lasting depolarization may be a somatic reflection of a high threshold dendritic calcium conductance activated by the sodium action potential, as has been reported in IB neurons (Chagnac-Amitai et al., 1990). However, injections of current pulses never evoked bursts in presumed pyramid-dependent burst neurons, unlike IB neurons. Furthermore, in IB neurons, as a burst developed during the rising time course of the underlying depolarization, the spike threshold increased and the spike amplitude decreased in association with an increment in the spike duration (McCormick et al., 1985
; Chagnac-Amitai et al., 1990
; Mason and Larkman, 1990
). These features of action potentials could be due to the inactivation of the sodium action potential which progressed during the rising time course of the underlying depolarization. In fact, similar burst neurons found in the cat motor cortex were categorized as inactivating bursting neurons (Baranyi et al., 1993
). In contrast, in presumed pyramid- dependent burst neurons, a burst developed during the decay time course of the long-lasting depolarization and the decrease in spike amplitude was not associated with an increment in the spike duration, unlike IB neurons. This suggests that the attenuation of spike amplitude in presumed pyramid-dependent burst neurons is not due to the inactivation of the sodium action potential, but presumably due to the shunting effect brought about by an increase in the conductance underlying the long-lasting depolarization. Furthermore, the burst in presumed pyramid-dependent burst neurons was followed by the long-lasting depolarization, whereas the burst in IB neurons was terminated by an AHP (McCormick et al., 1985
; Chagnac-Amitai et al., 1990
; Mason and Larkman, 1990
; Baranyi et al., 1993
). Thus, presumed pyramid-dependent burst neurons were distinct from IB neurons not only in morphological features (non- pyramidal versus pyramidal) but also in physiological properties.
Depolarizing Afterpotential
The presumed reversal potential (Erev = 43 mV) for the long-lasting depolarization is similar to that of Ca2+-dependent cation current (43 mV: Caeser et al., 1993; 40 mV: Kang et al., 1998
) and to that of Ca2+-independent cation current (48 mV; Alzheimer, 1994
). The former and latter cationic currents are considered to underlie slow and fast depolarizing afterpotentials (DAP) respectively. It may not be unreasonable to assume that the long-lasting depolarization following bursts is a kind of Ca2+-dependent slow DAP as synaptically induced spikes may involve more Ca2+ components than spikes evoked by current injections into the soma (Kim and Connors, 1993
). If this is the case, the peak level of the long-lasting depolarization should remain constant at the Erev in spite of varying membrane potentials. This is because the generation of the inward current responsible for the long-lasting depolarization begins when the spike is repolarized to more negative than the Erev of the cationic current (Alzheimer, 1994
). Recently, we have shown that the generation of the slow DAP in rat layer V pyramidal cells was mediated by a Ca2+-dependent cationic current (Erev = 40 mV) (Kang et al., 1998
), and the onset level of the slow DAP remained constant at the Erev regardless of the level of baseline membrane potentials (unpublished observation), as observed in presumed pyramid-dependent burst neurons in the present study (Fig. 7
).
An afterdepolarization following the first spike might have triggered the second spike which was also followed by another afterdepolarization that in turn triggered the next spike and so on, and resulted in a generation of burst after-discharge. Such an interdependent mechanism between spike and DAP would lead to concurrent fluctuations of the spike number during bursts and the half-duration of the long-lasting depolarization, without marked changes in the synaptic conductance or in the stimulus intensity (see Fig. 6D).
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Notes |
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Address correspondence to Y. Kang, Department of Physiology, Faculty of Medicine, Kyoto University, Kyoto 606, Japan. Email: ykang{at}med.kyoto-u.ac.jp.
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Appendix |
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where GS is a conductance induced by synaptic action, and Vm and Erev are the membrane potential and the reversal potential of EPSP respectively (Kandel and Schwartz, 1981). GS = 1/RS where R S is the shunting resistance at subsynaptic membrane. The net membrane current, Im is expressed as follows:
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where Cm is the membrane capacitance, R N is the input resistance of the neuron and Er is the resting membrane potential (Kandel and Schwartz, 1981). When there is no synaptic action, R S = (
GS = 0). If the membrane potential is displaced to Vh by passing a constant current Ih = (Vh Er)/RN under current-clamp condition, Im = Ih (constant). When synaptic action takes place, RS has a finite value. At the peak of EPSPs (Vmp), dVm/dt must be zero. Then:
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Thus, Vmp is somewhere in between Vh and Erev.
The amplitude of EPSPs (= Vmp Vh) is expressed as follows:
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The relation between Vh and EPSP amplitudes is represented by a straight line which has a slope of RN/(RN + RS) in a range between 1 and 0, intersecting at Erev (interrupted line in Fig. 7). When R S = 0, the amplitude of EPSPs is as large as the driving potential and the slope of the straight line is 1.
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