Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex.

Abstract

1. Dual intracellular recordings were made from synaptically coupled pyramidal cell-tointerneurone pairs (n = 5) of the cat visual cortex in vitro. Pre-and postsynaptic neurones were labelled with biocytin, followed by correlated light and electron microscopic analysis to determine all sites of synaptic interaction. 2. Pyramidal neurones in layers II-III elicited monosynaptic EPSPs in three distinct classes of smooth dendritic local-circuit neurones, namely basket cells (n = 3), a dendrite-targeting cell (n = 1) and a double bouquet cell (n = 1). Unitary EPSPs in basket cells were mediated by one, two, and two synaptic junctions, whereas the pyramid-to-dendrite-targeting cell and pyramidto-double bouquet cell interaction were mediated by five and seven synaptic junctions, respectively. Recurrent synaptic junctions were found on all somato-dendritic compartments, with a tendency to be clustered close to the soma on the double bouquet and dendrite-targeting cells. The latter interneurones were reciprocally connected with pyramidal cells. 3. Unitary EPSPs had an average peak amplitude of 1005 + 518 1sV, fast rise times (10-90%; 0-67 + 0-25 ms) and were of short duration (at half-amplitude, 4-7 + 1.0 ms). Their decay was monoexponential (T = 7-8 + 4-3 ms) at hyperpolarized membrane potentials and appeared to be shaped by passive membrane properties (T = 9-2 + 8-5 ms). All parameters of concomitantly recorded spontaneous EPSPs were remarkably similar (mean amplitude, 981 + 433 ,sV; mean rise time, 0-68 + 0-18 ms; mean duration, 4-7 + 1-7 ms). 4. In all three pyramidal-to-basket cell pairs, closely timed (10-50 ms) pairs of presynaptic action potentials resulted in statistically significant paired-pulse depression, the mean of the averaged second EPSPs being 80 + 11 % of the averaged conditioning event. The overall degree of paired-pulse modulation was relatively little affected by either the amplitude of the preceding event or the inter-event interval.5. The probability density function of the peak amplitudes of the unitary EPSPs could be adequately fitted with a quantal model. Without quantal variance, however, the minimum number of components in the model, excluding the failures, exceeded the number of electron microscopically determined synaptic junctions for all five connections. In contrast, incorporating quantal variance gave a minimum number of components which was compatible with the number of synaptic junctions, and which fitted the data equally well as models incorporating additional components but no quantal variance. For this model with quantal variance with the minimum number of components the estimate of the quantal coefficient of variation ranged between 0 33 and 0-46, and the corresponding quantal sizes ranged between 260 and 657 ,sV. The peak EPSP amplitudes in two of the four connections with more than one synaptic junction could be adequately described by a uniform binomial model for transmitter release. 6. In conclusion, at least three distinct interneurone classes receive local excitatory pyramid...

Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses

“…The number of EMdetermined synaptic junctions in the examined connections (N EM ) ranged between one and six, with a mean of 2.8 Ϯ 0.8 (n ϭ 6) ( Table 1). Our result is in agreement with several reports demonstrating that hippocampal and cortical PCs and dentate gran- ule cells excite their target INs through few release sites (ranging from 1 to 7) (Gulyas et al, 1993;Buhl et al, 1997;Geiger et al, 1997;Lawrence et al, 2004).…”

“…Possibly an even more successful avenue has been the combination of electrophysiological recordings with either anatomical or imaging techniques. For example, paired recordings with subsequent light microscopic (LM) and electron microscopic (EM) analysis of the number of synaptic contacts have been successful approaches to obtain independent estimates of N (Korn et al, 1982;Gulyas et al, 1993;Buhl et al, 1997;Silver et al, 2003). Alternatively, two-photon imaging of calcium transients in single spines (Oertner et al, 2002;Nimchinsky et al, 2004) and imaging of the destaining rate of FM1-43 fluorescence (Murthy et al, 1997) have been used to monitor P r independently of electrophysiological recordings.…”

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

“…We identified 32 autapses on a DTC, which represent the highest number of transmitter release sites so far on a single cortical cell originating from an individual axon of any origin (e.g., see Freund et al, 1985;K isvárday et al, 1987;Deuchars et al, 1994;Thomson et al, 1996;Buhl et al, 1997). The formation of autapses is both cell type-specific and selective with regard to the placement of autapses on specific subcellular domains.…”

“…B, Synaptic and autaptic relationships between a layer IV DTC (soma and dendrites, red; axon, black) and a layer III-IV border pyramidal cell (soma and dendrites, green; axon, blue). The complete axonal and dendritic arborizations are shown by Buhl et al, (1997, their Fig. 1).…”

“…5B). Only the EPSPs, elicited by the pyramidal cell via five synapses, were measured in the DTC (for the recordings and complete axonal and dendritic arbors, see Buhl et al, 1997, their Fig. 1).…”