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Department of Physiology, Faculty of Health Sciences, Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel
Submitted 24 February 2004; accepted in final form 8 July 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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). Confusion, drowsiness, dizziness, and impairment of cognitive skills are frequent expressions of this disorder (for a review, see Jain 1994). Disturbances of memory and intellectual operation (Abraini 1997; Logue et al. 1986; Overman et al. 1989; Steevens et al. 1999; Vaernes et al. 1988) and of locomotor activity (Darbin et al. 2000; Tarasiuk and Grossman 1990) generate significant dysfunction and danger to humans working at high pressure. More severe manifestations, such as myoclonia (Darbin et al. 2000), convulsions, and death, were observed in experimental animals exposed to hyperbaric conditions (for review, see Bennett and Rostain 2003). The progressive occurrence of neurological signs is associated with increasing hyperexcitability in the electroencephalogram (EEG) (Bennett and Rostain 2003; Rostain et al. 1997; Vaernes et al. 1982) and evoked potentials (Harris et al. 1985; Lorenz et al. 1995; Vaernes and Hammerborg 1989). The mechanisms affecting human cognitive function at pressure are not yet clear but seemingly are generated by network dysfunction at respective cerebral areas (Abraini 1997). Learning and memory are related to the function of corticohippocampal areas in primates (Scoville and Milner 1957; Squire and Zola-Morgan 1991; Zola-Morgan et al. 1982) and in rats (Ferbinteanu et al. 1999; Quirk et al. 1992). Normal communication between the medial entorhinal cortex and the dentate gyrus (DG), the first station in the corticohippocampal circuit, is frequency dependent, displaying low-pass filter properties (Dreier and Heinemann 1991). The medial perforant pathway (MPP) conveys this connection (Swanson and Kohler 1986), and its synapses on granule cells (GC) show frequency-dependent depression (FDD) when stimulated at frequencies >1 Hz (Kilbride et al. 2001). Recently, we have demonstrated a significant depression in the performance of these synapses under high-pressure conditions. Single inputs of the MPP synapse (Talpalar and Grossman 2003) as well as the Shaffer collateral synapse at the CA1 area of the hippocampus (Fagni et al. 1987a), were severely depressed under high pressure. This depression of single synaptic events was associated with increased paired-pulse facilitation (Talpalar and Grossman 2003). Previous studies in invertebrate synapses showed increased facilitation (Campenot 1975; Golan and Grossman 1992) as well as enhanced tetanic and posttetanic potentiation (Grossman and Kendig 1988, 1990). In contrast, although high pressure increased facilitation in the MPP synapses, stimulation at frequencies (25–50 Hz) resulted, respectively, in conserved or even increased FDD (Talpalar and Grossman 2003). These synaptic modifications may alter the filter properties of the DG and consequently disrupt the normal decoding of entorhinal cortex firing by the GCs. This may result in altered memory acquisition (Moser and Andersen 1994) or even induce hippocampal seizures at the seizure-prone CA3 area (Scharfman and Schwartzkroin 1990), which is innervated by the GCs. Weakening of synaptic inputs seems paradoxical in view of the obvious signs of hyperexcitability during the HPNS. We used electrophysiological techniques in rat corticohippocampal slices to investigate the effect of high pressure of helium on the excitability of DG's GCs as a model for HPNS. For this purpose, we compared population spike generation in response to synaptic activation of the MPP and the antidromic stimulation of GCs axons during single and frequency stimulation. |
METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Sprague-Dawley rats of both sexes (150–250 g) were killed (pentobarbital, 60 mg/kg); their brain was extracted (<1 min) and submerged in cold Ringer solution (4–6°C). Corticohippocampal slices (400 µm) were prepared as previously described (Dreier and Heinemann 1991; Talpalar and Grossman 2003). Slices were cut in a horizontal vibratome (Campden Instruments) and conserved in an incubation chamber at 25°C for later utilization. Regular Ringer solution contained (in mM) 124 NaCl, 3 KCl, 2 CaCl2, 2 MgSO4H, 1.25 NaH2PO4, 26 NaHCO3, and 10 D-glucose. Solution was constantly bubbled with 95% O2-5% CO2 for a pH of 7.4.
Pressure and compression
Electrophysiological experiments were carried out in a pressure chamber (Canty Assoc.). The chamber was provided with an internal experimental bath containing a pair of stimulation electrodes and a temperature gauge. The slice, lying on the surface of the bath, was superfused with prewarmed Ringer solution. A remote-controlled manipulator allowed the placement of the recording pipette in different areas of the corticohippocampal slice (Talpalar and Grossman 2003). Hyperbaric pressure was attained by compressed helium, a gas that is chemically inert at these pressures (0.1–10.1 MPa). Some of the controls were taken at 0.2–0.4 MPa because these small pressures were more stable than at 0.1 MPa for further pressurization. Although a small population of medullary neurons was shown to be sensitive to these small pressures (Dean and Mulkey 2000), they did not significantly modified field potential recordings in corticohippocampal slices (Talpalar and Grossman 2003) and cerebellar preparations (Etzion and Grossman 2000). Rates of compression-decompression varied between 0.15 and 0.2 MPa/min. Samples were taken at control (0.1–0.4 MPa) and 5.1 and 10.1 MPa. Ringer solution (saturated at normal pressure with 95% O2-5% CO2) was injected into the experimental bath by a fast high-pressure pump (LDC analytical minipump). To avoid transient effects of pressure (Grossman and Kendig 1984), samples were collected under strict conditions of temperature (30°C) and at least after 15–20 min of stable recording. This time excludes the time needed for stabilization of temperature transients of ±2°C during the processes of compression-decompression (
32 and 28°C, respectively). Decompression was routinely attempted to prove reversibility of high-pressure effects. Complete recovery was attained during decompression from 10.1 to 5.1 MPa in all the experiments, whereas almost complete recovery was observed in decompression from 5.1 to 0.4 MPa. Decompression <0.4 MPa was only successful in 
50% of the experiments (in which this final step of decompression was performed extremely slowly).
Electrophysiological recordings
Extracellular field potentials were recorded at the somatic (Fig. 1C) and at the inner dendritic areas (Fig. 1B) of the DG using glass micropipettes (1.5–3 M
) filled with Ringer solution (Fig. 1A). Tungsten bipolar stimulating electrodes were placed either at the subiculum or the inner dendritic area of the DG for stimulating the MPP (Fig. 1A). Output/input curves were plotted using standardized stimulus-intensities (usually 4–5 steps, if not otherwise expressed) between the threshold intensity and the saturation level. The latter involved a set of experiments in which population spike (PS) amplitude was plotted as a function of field excitatory postsynaptic potential (fEPSP) of different amplitudes (6–10 intensities of stimulus) under control and experimental pressures.
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Data analysis
Synaptic recordings of MPP fEPSPs at the inner dendritic region of the DG, its parameters, and their interpretation, were described elsewhere (Talpalar and Grossman 2003). In brief, fEPSP's amplitude, indicating inward synaptic currents, and fEPSP's slope expressing the rate of activation of synaptic receptors were used in these experiments for assessing synaptic activity. fEPSP's slopes were commonly used because they are more reliable than fEPSP's amplitude as a parameter for evaluating synaptic activation (Fagni et al. 1987a; Talpalar and Grossman 2003). GC excitability at high pressure was assessed in two ways: by generation of PS in response to MPP fEPSPs and by the induction of AAPs. The first describes the integrative capacity of the GC in response to synaptic activation; the second roughly delineates the general ability of GC to elicit spikes. Two different protocols were used for studying excitability at frequencies: paired-pulse stimulation and multiple stimuli. Pairs of stimuli, with 10- to 100-ms interstimulus-interval (ISI), were delivered every 20 s. Slope of both fEPSPs in the pair, E1 and E2, and the PS generated were compared. Results were plotted at the normalized form E2/E1 and PS2/PS1 for each ISI. Paired-pulse depression (PPD) and paired-pulse facilitation (PPF) were used for describing respectively relative decrease or increase of E2 with respect to E1. The expression paired-pulse modulation (PPM; negative or positive) was used as a generic term. Trains of five impulses at frequency (25–50 Hz), delivered at a rate of one train per minute, were applied to the orthodromic afferent fibers (MPP) and antidromically to the mossy fibers. Analysis of these responses involved the measurement and comparison of each response in the train at each frequency and the comparison of the effect of frequency on amplitude, integral, or rates. Events were usually normalized with respect to the first event. We attempted to fit the observed patterns with mathematical functions (e.g., exponential decay) to be used for comparison under various conditions. Frequency-dependent potentiation (FDP), frequency-dependent depression (FDD) and the generic term frequency-dependent modulation (FDM; positive or negative) were used for such synaptic behaviors.
The results of these experiments unless otherwise stated are expressed as means ± SE. The n expresses the number of slices successfully used in each experimental protocol. Given the time-consuming experiments at hyperbaric pressure usually just a single slice from each animal could be successfully used per experiment. Statistical tests were used for comparing the effect of various conditions on the electrophysiological signals (slope, amplitude, time constant, etc.). Student's t-test for paired observations was used for comparing parameters at control and under experimental conditions in the same slice/experiment. ANOVA tests (1-way independent and for repetitive measurements) were used for comparing independent results and sets of stimuli at frequency. Degree of significance was indicated by values of P (results were considered statistically different for P < 0.05).
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RESULTS |
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The MPP input innervates the proximal dendrites of the GCs. Spike generation by the GCs depends on their threshold for action potential and on the amplitude of MPP synaptic potentials that activate them. Because MPP fEPSP's slope is depressed by 20% at 5.1 MPa and by 55% at 10.1 MPa (Talpalar and Grossman 2003), we had to normalize the synaptic input to evaluate these cells' excitability.
As a first approximation, we compared PS generation by fEPSPs the slopes of which at high pressure were matched to control fEPSP's slope by increasing the stimulus intensity or duration. PS amplitude at pressure was significantly greater than that generated by equal fEPSPs at 0.1 MPa (Fig. 2A). For example, a just-suprathreshold fEPSP at 0.1 MPa generated a PS of 0.22 ± 0.21 mV, a fEPSP of the same slope induced PSs of 0.94 ± 0.29 mV at 5.1 MPa (n = 9; P < 0.002) and of 0.73 ± 0.21 mV at 10.1 MPa (n = 9, P < 0.05).
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Despite the pressure depression of the MPP fEPSPs (as in the preceding text), the PSs generated under these stimulus and pressure conditions were not significantly different from controls (see Table 1).
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), it seems that corticohippocampal transmission code for single response is kept "constant" due to some "compensation" mechanism. To characterize this process more precisely, we stimulated the MPP with 10 different stimulus intensities (Fig. 3A) and normalized the synaptic transfer function by plotting PS amplitudes as a function of the fEPSPs' slopes (Fig. 3B). This input/output plot shifted to the left at pressure, indicating hyperexcitability of the GCs. Namely, similar PSs could be elicited with smaller fEPSP under pressure conditions.
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As suggested in the preceding text, the increase in the PS excitability may arise form changes in the action potential firing capability of the GCs. Therefore we examined the effects of pressure on antidromically evoked action potentials in these cells (Fig. 4A), a method that does not involve any synaptic activation. Pressure effects on the AAP are summarized in Fig. 4B. Increasing pressure from 0.1 to 5.1 MPa and to 10.1 MPa reduced AAP initial slope by 28 and 29%, respectively. The slope of decay of AAP was not statistically different at 5.1 MPa and showed a trend toward reduction by 16% at 10 MPa. AAP's duration was prolonged by 21% at 5.1 MPa and by 20.4% at 10.1 MPa. The amplitude of the AAP at 5.1 MPa and at 10.1 MPa was not statistically different from controls. APP integral was almost constant at the three different pressures (Fig. 4). The small-amplitude reduction of AAPs under hyperbaric conditions seems to be a direct effect on the kinetics of the action potential. Reduction of the AAP's initial slope may be interpreted as a slowing down of the kinetics of activation of the Na current responsible for the rising phase of the action potential, whereas the maintained or slightly increased decay rate suggests a small effect on the inactivation of Na currents and/or on the kinetics of K currents responsible for the decay of action potentials (Kendig 1984). The small depression of AAP amplitude and specially the lack of effect on AAP's integral suggest that the effect of pressure on the amplitude of the action potential or on the total number of recruited fibers was minimal and, if at all, it was depressive.
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The initial slope of a single fEPSP is the cleanest parameter for evaluating the synaptic input at the dendrites, while fEPSP's amplitude may also reflect the currents developed by recruitment of a voltage-dependent component. We compared these parameters for estimating the effects of pressure on a voltage-dependent boosting of the fEPSP. Plotting fEPSP's amplitude as a function of fEPSP's initial slope resulted in a steeper slope of the fEPSP's amplitude/slope relationship at high pressure (n = 17). This suggests that synaptic inputs were either more efficiently conducted through the dendrites, or maybe even slightly amplified under such condition (Fig. 4C).
Increased GC excitability maintains PS firing during MPP paired-stimulation at high pressure
Paired-pulse stimulation to the MPP resulted in a couple of fEPSPs in the GCs (E1 and E2), the second one eliciting a PS with greater amplitude. We termed this behavior paired-pulse transfer (PPT). Under control conditions, PPT extended from ISIs of 10 to 120 ms. The greatest PPT occurred at ISIs between 10 and 40 ms (Fig. 5, A and B). As we recently reported, high pressure depressed single E1 while increasing synaptic facilitation of E2, but the absolute size of synaptic inputs was smaller than the control (Talpalar and Grossman 2003). The time pattern of control PPT did not significantly change at 5.1–10.1 MPa pressure in spite of depression of synaptic inputs (Fig. 5C). Furthermore, two additional experiments extending the ISI range to 200 ms did not show significant difference in PPT (not shown).
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Increasing the stimulus intensity of E1 at 5.1 and 10.1 MPa to match the amplitude of control E1 produced a PS1 that was larger than controls (similar to that described for single stimulus), whereas the PS2 brought about during paired-pulse stimulation, for example at 20 ms ISI, was larger than that generated at 0.1 MPa (Fig. 5D).
High pressure increases DG excitability during stimulation at frequency
As we have recently shown (Talpalar and Grossman 2003), stimulation of the MPP with short trains at frequencies of 10–100 Hz elicited fEPSPs that showed a variable degree of facilitation of E2 and then followed by progressively decaying E3–5 as a function of frequency and use. This FDD of the fEPSPs was modulated by high pressure: at 25 Hz, FDD was not significantly altered, whereas at 50 Hz, it was increased. Similarly, under control conditions, stimulation at 25–50 Hz generated the largest PS at E2 (PPT, as described in the preceding text), whereas amplitudes of PSs induced by the following En decayed as a function of time and frequency (Fig. 6). We termed this phenomenon frequency-dependent attenuation (FDA) of the PS.
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), while later FDA of the following responses in the train is possibly the result of GABAA inhibition (Golan et al. 1996; Buckmaster and Dudek 1997). We therefore tested whether the reduction of FDA at 50 Hz may result from decreased inhibition at the DG. Partial blockade of GABAA inhibition with low-dose bicuculline methyiodide (BMI, 0.3 µM) mimicked pressure effect on FDA (Fig. 9, A and B). Moreover, in presence of high dose of BMI (10 µM) high pressure did not further increase GC excitability during trains at 50 Hz but rather decreased it (n = 2; Fig. 9C). This suggests that hyperexcitability at high pressure partially involves synaptic depression of inhibitory pathways.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Pressure effects of synaptic inputs per se confirmed our recent report (Talpalar and Grossman 2003). In short, at 10.1 MPa, single MPP fEPSPs were depressed by 50%. These events displayed longer synaptic delay and prolonged time course. Paired-pulse protocols resulted in depression of the first fEPSP (E1) and in relative reduction of PPD at short ISIs (10 to <40 ms) and in some degree of PPF at ISIs of between >40 and 120 ms. In spite of less PPD and larger PPF, the absolute second fEPSP (E2) at high pressure remained smaller than controls. The effect of high pressure on short-term synaptic plasticity depended on the frequency of stimulation: trains of five stimuli at 25 Hz displayed the same rate of FDD, whereas stimulation at 50 Hz displayed greater FDD (Talpalar and Grossman 2003). This resulted in relatively conserved E5 at 25 Hz and in further depression of this response at 50 Hz. Regarding the efficacy of fEPSPs at high pressure, the present experiments show that for single fEPSP the amplitude/slope relationship tended to increase at high pressure.
GCs excitability
GCs, in spite of the pressure depression of synaptic inputs, supported regular spike firing in response to a single MPP synaptic stimulus. Adjustment of the pressure-depressed synaptic inputs to control levels resulted in significant enhancement of population spike generation. These results indicate increased excitability of the GC. The maximal absolute amplitude of PS induced by any standardized fEPSP often occurred at 5.1 MPa. At 10.1 MPa, the amplitude of PS induced by a similar stimulus-intensity tended to be reduced presumably because of the extreme synaptic depression and the temporal dispersion of the PS. However, the PS/fEPSP relationship continued rising while increasing pressure (Fagni et al. 1987a). AAPs showed a pressure-resistant integral, a slightly reduced amplitude, and prolonged initial slope and duration. Stable integral suggests that the total number of recruited fibers was not changed. This means that changes in threshold and action potential amplitude may be minor. These findings are in accord with our recent report of minor effects of pressure in the main axons and presynaptic volley of MPP axons in the same system (Talpalar and Grossman 2003). Pressure-enhancement of excitability of CA1 pyramidal cells was also paradoxically correlated with depression of both synaptic inputs and antidromic action potentials (Fagni et al. 1987a). In addition, action potentials of CA1 pyramidal cells were also not significantly affected by pressure as shown by intracellular recordings (Southan and Wann 1991, 1996). Slow AAP rates may result from slowing down of the kinetics of individual action potentials and also by their unsynchronized recruitment. Differential effects on the conduction velocity of different kind of axons (Grossman and Kendig 1984) may result in unsynchronized AAPs. Slowing down of Na+ and K+ currents kinetics may induce these effects (Conti et al. 1982a, b; Grossman and Kendig 1984; Harper et al. 1981; Heinemann et al. 1987). Increased GC excitability in spite of synaptic depression and small changes in action potential suggests that pressure affects dendritic integrative properties. Hyperexcitability may be induced by intrinsic "boosting" mechanism(s) or reduced tonic inhibition (see following text) at strategic regions of the dendrites (Faber and Korn 1986; Fagni et al. 1987a). The shift in the relationship between fEPSP's slope and amplitude at high pressure may suggest boosting (Fagni et al. 1987a). Although lengthening of the decay time constant of EPSPs at pressure may reflect general effects on excitatory synapses (Ashford et al. 1982), the highly pressure-sensitive lengthening of fEPSP's 
decay (Talpalar and Grossman 2003) may indicate increase of the NMDA receptor (NMDA-R) component (Fagni et al. 1987b; Roberts et al. 1996; Wardley-Smith and Wann 1989) or alternatively activation of voltage-dependent channels (Faber and Korn 1986; Harper et al. 1981; Stuart and Sakmann 1995). Action potential generation at the dendrites (Stuart and Sakmann 1994; Stuart et al. 1997a, b) and boosting of EPSPs by voltage-dependent currents have been observed in pyramidal cells of the neighboring CA1 (Spruston et al. 1995) and CA3 areas (Buzsaki et al. 1996) of the hippocampus as well as in other neurons (Hausser et al. 1995). Although these phenomena have not yet been studied in DG GCs, they are probably present in these cells and may influence the EPSP-to-spike transfer. Because the antidromic spikes (AAPs) were unchanged or even depressed at high pressure, it is inferred that there were no changes toward hyperexcitability at the somata of these cells. Because the soma is the area where tonic inhibition was postulated to exert its most prominent effects (Soltesz et al. 1995), it is also speculated that the effects of pressure on tonic inhibition were not very relevant.
Feedforward inhibition, affecting the efficacy of perforant path inputs at the GCs has also been described at the DG (Kneisler and Dingledine 1995). The GABAA-mediated component of this input induces a shunt that decreases the late NMDA-dependent phase of the EPSP without affecting its early AMPA-mediated phase (Staley and Mody 1992). In spite of this effect, application of GABAA blocker to the present preparation (see E1 in Fig. 9, B and C) failed to produce relevant effects on PS generation by a single stimulus. This lack of disinhibition may have resulted from disconnection of the MPP pathway that activates the inhibitory neurons due to the angle of slicing. Thus probably the maintenance of PS generation by a single fEPSP may be attributed to changes in the membrane-passive properties, the kinetics of voltage-dependent conductances, and/or NMDA-R activation. However, a more powerful feedforward inhibition, in the CA1 area of the hippocampus, was shown to decrease under high-pressure conditions (Zinebi et al. 1988). Because activation of feedforward inhibition at the DG requires recruitment of at least two synaptic inputs, it is likely that inhibition will be more susceptible to high-pressure effects than excitatory inputs. Therefore we cannot exclude some contribution of reduced feedforward inhibition to pressure-induced hyperexcitability.
Frequency response
Despite that pressure depressed paired fEPSPs, the PSs induced by them were similar to control indicating increased excitability of the GCs. Likewise, conserved spike generation was observed during stimulation with trains at 25 Hz. Trains of fEPSPs at higher frequency (50 Hz), however, showed roughly preserved PS1–2 but enhanced PS3–4, indicating hyperexcitability and disruption of the low-pass filter properties of the DG. This means that although this system copes quite well with the effects of high pressure at single stimulus and low-frequency responses, it fails to do so at high frequencies.
The regular mechanism for limitation of action potential generation by GC involves activation of recurrent inhibition by hilar interneurons (Gulyas et al. 1993). This mechanism was apparently altered at high pressure (Zinebi et al. 1988) probably as a result of general synaptic depression. This may allow PS generation also at later events (PS3–4) during the train. Partial blockade of GABAA inhibition reproduced this effect, suggesting that pressure was partially blocking fast inhibitory function (Roberts et al. 1996; Zinebi et al. 1990). Furthermore, the fact that high pressure did not enhance PS generation at high frequency when fast inhibition was previously blocked suggests that enhanced excitability is, at least partially, due to GABAA inhibition failure. This effect may result from proportional reduction of synaptic inputs (mostly involving activation of >2 synapses) necessary for the inhibitory function. Frequency dependence may be explained by slowed kinetics and conduction at high pressure leading to delayed inhibitory influences.
Increased excitability: an adaptive mechanism?
Changes induced by pressure in the PS/fEPSP relation at the low-frequency range seem to be an adaptive stabilizing mechanism. High pressure progressively depresses synaptic inputs while it increases excitability of the circuit. This is unlikely to induce the large hyperexcitability described in HPNS. The reliability of this mechanism may be challenged by extremes of intensity and frequency of neuronal activity. Transfer of regular activity from the cortex to the DG may be impaired if too depressed synaptic inputs cannot reach action potential threshold. However, highly synchronized activity and high frequency may easily spread through the DG to the CA3–CA1. Thus in some circumstances, pressure-induced changes may impair normal network function while favoring spread of anomalous activity. The postulated postsynaptic boosting of presynaptically depressed inputs may be interpreted as an adaptive strategy of the system for maintaining neural transmission under progressively lower incoming signals (Abraham and Bliss 1985).
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FOOTNOTES |
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Address reprint requests and other correspondence to: Y. Grossman (E-mail: ramig{at}bgumail.bgu.ac.il).
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REFERENCES |
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, the amplitude of the PS used for the analysis of these events. C: somatic recording at the GCs layer of an MPP fEPSP that generated a large PS. Parameters for analysis here are the PS's delay (1) and amplitude (2). D: antidromic action potential (AAP) recorded at the GC layer of the DG. AAP parameters for analysis are delay (1), amplitude (2), slope (3), duration (4), and the integral.
) by a train in response to MPP synaptic stimulation at 50 Hz. B: similar recordings at atmospheric pressure show occurrence of later spikes at PS3–4 after the progressive effect of bicuculline methyiodide (BMI 0.3 µM). C: application of GABAA blocker (BMI 10 µM) significantly increases GC excitability during stimulation at 50 Hz (top). When this kind of inhibition has been blocked, high pressure not only does not increase (5.1 MPa) but also depresses (10.1 MPa) PS generation (