Slower spontaneous excitatory postsynaptic currents in spiny versus aspiny hilar neurons

Livsey, Charles T.; Vicini, Stefano

doi:10.1016/0896-6273(92)90095-u

Cited by 53 publications

(61 citation statements)

References 43 publications

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“…8). This percentage was low compared to other dentate interneurons impaled in the hilar region (Livsey and Vicini, 1992) and other non-granule cells such as mossy cells (Fig. 8).…”

Section: Synaptic Potentials and Responses To Stimulation Of The Slicementioning

confidence: 98%

“…This suggests that the underlying EPSPs of pyramidal-shaped cells and granule cells may differ mechanistically, such as in the receptors that are activated or the ions involved. Livsey and Vicini have identified differences in glutamate receptors on interneurons in the hilar region (Livsey and Vicini, 1992). An alternative explanation is that there could be differences in the number of excitatory synapses on the different cells.…”

Section: Types Of Responsesmentioning

confidence: 99%

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Electrophysiological diversity of pyramidal‐shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro

Scharfman

1995

Hippocampus

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In the rat dentate gyrus, pyramidal-shaped cells located on the border of the granule cell layer and the hilus are one of the most common types of γ-aminobutyric acid (GABA)-immunoreactive neurons. This study describes their electrophysiological characteristics. Membrane properties, patterns of discharge, and synaptic responses were recorded intracellularly from these cells in hippocampal slices. Each cell was identified as pyramidal-shaped by injecting the marker Neurobiotin intracellularly (n = 17).In several respects the membrane properties of the sampled cells were similar to "fast-spiking" cells (putative inhibitory interneurons) that have been described in other areas of the hippocampus. For example, input resistance was high (mean 91.3 megohms), the membrane time constant was short (mean 7.7 ms), and there was a large afterhyperpolarization following a single action potential (mean 10.5 mV at resting potential). However, the action potentials of most pyramidalshaped cells were not as brief (mean 1.2 ms total duration) as those of most previously described fast-spiking cells. Many pyramidal-shaped neurons had strong spike frequency adaptation relative to other fast-spiking cells. Although these latter two characteristics were apparent in the majority of the sampled cells, there were exceptional pyramidal-shaped neurons with fast action potentials and weak adaptation, demonstrating the electrophysiological variability of pyramidal-shaped cells.Responses to outer molecular layer stimulation were composed primarily of excitatory postsynaptic potentials (EPSPs) rather than inhibitory postsynaptic potentials (IPSPs), and were usually small (EPSPs evoked at threshold were often less than 2 mV), and brief (less than 30 ms). There was variability, because in a few cells EPSPs evoked at threshold were much larger. However, regardless of EPSP amplitude, suprathreshold stimulation (up to 4 times the threshold stimulus strength) rarely evoked more than one action potential in any cell. The results suggest that stimulation of perforant path axons produces limited excitatory synaptic responses in pyramidal-shaped neurons. This may be one of the reasons why they are relatively resistant to prolonged perforant path stimulation.The pyramidal-shaped neurons located at the base of the granule cell layer have been associated historically with a basket plexus around granule cell somata, and have been called pyramidal "basket" cells. However, basket-like endings were rare and axon collaterals outside the granule cell layer were common. Many axon collaterals were as far from the granule cell layer as the outer molecular layer and the central hilus, and antidromic action potentials could be recorded in some

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“…8). This percentage was low compared to other dentate interneurons impaled in the hilar region (Livsey and Vicini, 1992) and other non-granule cells such as mossy cells (Fig. 8).…”

Section: Synaptic Potentials and Responses To Stimulation Of The Slicementioning

confidence: 98%

Section: Types Of Responsesmentioning

confidence: 99%

Electrophysiological diversity of pyramidal‐shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro

Scharfman

1995

Hippocampus

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“…In this respect, the similarity of the decay of NMDA EPSCs in PCs and dentate granule cells (Table 1), which also bear spines on their dendrites (Ribak, Seress & Amaral, 1985), raises the possibility of spine filtering. Interestingly, it was recently found in the rat hippocampal hilus, that non-NMDA EPSCs are significantly slower in spiny versus aspiny neurones (Livsey & Vicino, 1992). However, current kinetics are not expected to change according to some spine models (Koch & Poggio, 1983 Mechanism of the slow NMDA EPSC Several mechanisms may possibly cause the unusually slow NMDA EPSC.…”

Section: Discussionmentioning

confidence: 99%

Kinetic properties of NMDA receptor‐mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones.

Perouansky

Yaari

1993

The Journal of Physiology

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4. In saline containing 1 mM Mg2+, the peak current-voltage (I-V) relationship of NMDA EPSCs in PCs and INs showed an area of negative slope conductance at voltages more negative than -20 to -30 mV. In nominally Mg2+-free saline, the peak I-V relation was linear over a much wider voltage range in both cell types.5. The 10-90 % rise times of NMDA EPSCs at -60 mV ranged from 4-5 to 16 ms in PCs (mean 8-7 ms; n = 25) and in M-INs (mean 9-1 ms; n = 10). Their decay could be best fitted with the sum of two exponentials. The 6. The time course of NMDA EPSCs in OA-INs (n = 37) was considerably more variable. In 18 9 % of the cells the rise times were in the ordinary range (4 5-10 nms: mean 6 9 ms) and the decay was biexponential (mean Tf and Ts8 49 and 212 ms: mean Af and As, -76'3 and -137'2 pA, respectively). In 73% of OA-INs the rise times were very slow (18-53 ms: mean 31-2 ms) and decayed monoexponentially (mean time constant 217 2 ms). The remaining 8% had rise times in the ordinary range (10-14 ms: mean 117 ms) but decayed as a single exponential (mean time constant 226 ms).7. Changes in holding voltage had no systematic effect on rise time and decay of ordinary and slow NMDA EPSCs.8. Neither changing the site of stimulation, nor modulating the amount of glutamate release by varying stimulus intensity, lowering extracellular Caa2+ or adding Cd21 to the saline, affected the rise time or the decay of slow NMDA EPSCs.9. We conclude that PCs and INs in area CAI of the rat hippocampus express NMDA EPSCs with different kinetic characteristics. NMDA EPSCs in the majority of OA-INs display unusually slow rise times.

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“…Intense and continuous spontaneous excitatory synaptic activity has been reported in both AHIs and SMCs Scharfman, 1991;Livsey and Vicini, 1992). There is a difference in the kinetics of spontaneous excitatory postsynaptic currents (sEPSCs) between AHIs and SMCs in the hippocampal hilus (Livsey and Vicini, 1992).…”

mentioning

confidence: 99%

“…There is a difference in the kinetics of spontaneous excitatory postsynaptic currents (sEPSCs) between AHIs and SMCs in the hippocampal hilus (Livsey and Vicini, 1992). sEPSCs in AHIs (n = 48) are much faster (mean rise time = 0.5 -t 0.2 msec, mean decay time constant = 3.6 f 1.5 msec, mean + SD) than those in SMCs (n = 55, mean rise time = 1.0 + 0.3 msec, mean decay time constant = 9.6 ?…”

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confidence: 99%

Glutamate-activated currents in outside-out patches from spiny versus aspiny hilar neurons of rat hippocampal slices

1993

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The desensitization rate of non-NMDA glutamate receptors was investigated in outside-out membrane patches obtained from morphologically identified spiny “mossy cells” (SMCs) and aspiny hilar interneurons (AHIs) in young rat hippocampal slices. The fast application of a 1 mM step of L-glutamate for 50–100 msec in the presence of TTX and dizolcipine (MK-801) onto patches excised from these neurons produced large glutamate-activated currents (GACs) that decayed with a single or double exponential time course despite the continued presence of agonist. These desensitization rates of alpha- amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate- sensitive receptors differed markedly between patches obtained from the two cell types. The fast time constant of desensitization in AHIs (n = 34) averaged 3.3 +/- 0.93 msec (mean +/- SD), while that of SMCs (n = 57) averaged 6.8 +/- 2.0 msec. Current-voltage relationships of the GACs did not differ between SMCs and AHIs, with comparable reversal potentials and no evidence of inward rectification. We also failed to observe significant Ca2+ permeability in either cell type. However, brief (< 1 msec) pulses of 1 mM glutamate produced rapidly decaying GACs with distinct kinetics in the two neuronal classes. Furthermore, analysis of the single glutamate-activated channel currents in outside- out patches from hilar neurons revealed a larger predominant single- channel current in AHIs versus SMCs. Lastly, we observed a greater sensitivity to cyclothiazide in SMCs versus AHIs, with half-maximal removal of desensitization being 90 mM and 200 mM, respectively. Taken together, these differences in GACs between SMCs and AHIs might indicate a functional correlate to the substantial heterogeneity in the molecular structure of glutamate receptor subunits or might be related to posttranslational modifications of these subunits, perhaps provided by the unique microenvironment in the spines covering SMCs.

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Slower spontaneous excitatory postsynaptic currents in spiny versus aspiny hilar neurons

Cited by 53 publications

References 43 publications

Electrophysiological diversity of pyramidal‐shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro

Electrophysiological diversity of pyramidal‐shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro

Kinetic properties of NMDA receptor‐mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones.

Glutamate-activated currents in outside-out patches from spiny versus aspiny hilar neurons of rat hippocampal slices

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