FAST IPSPS ELICITED VIA MULTIPLE SYNAPTIC RELEASE SITES BY DIFFERENT TYPES OF GABAERGIC NEURON IN THE CAT VISUAL-CORTEX

1. The effects of synapses established by smooth dendritic neurones on pyramidal and spiny stellate cells were studied in areas 17 and 18 of the cat visual cortex in vitro. Paired intracellular recordings with biocytin-filled electrodes and subsequent light and electron microscop ic analysis were used to determine the sites of synaptic interaction. 2. All smooth dendritic cells established type II synapses previously shown to be made by terminals containing GABA, therefore the studied c ells are probably GABAergic. Three classes of presynaptic cell could b e defined, based on their efferent synaptic target preference determin ed from random samples of unlabelled postsynaptic cells. (a) Basket ce lls (n = 6) innervated mainly somata (49.9 +/- 13.8%) and dendritic sh afts (45.2 +/- 10.7%) and, to a lesser extent, dendritic spines (4.9 /- 4.6%). (b) Dendrite-targeting cells (n = 5) established synapses pr edominantly on dendritic shafts (84.3 +/- 9.4%) and less frequently on dendritic spines (11.2 +/- 6.7 %) or somata (4.5 +/- 4.7%). (c) Doubl e bouquet cells (n = 4) preferred dendritic spines (69.2 +/- 4.2%) to dendritic shafts (30.8 +/- 4.2%) as postsynaptic targets and avoided s omata. 3. 3. Interneurones formed 5240 +/- 1600 (range, 2830-9690) syn aptic junctions in the slices. Based on the density of synapses made b y single interneurones and the volume density of GABAergic synapses, i t was calculated that an average interneurone provides 0.66 +/- 0.20% of the GABAergic synapses in its axonal field. 4. The location of syna ptic junctions on individual, identified postsynaptic cells reflected the overall postsynaptic target distribution of the same GABAergic neu rone. The number of synaptic junctions between pairs of neurones could not be predicted from light microscopic examination. The number of el ectron microscopically verified synaptic sites was generally smaller f or the dendritic domain and larger for the somatic domain than expecte d from light microscopy. All presynaptic cells established multiple sy naptic junctions on their postsynaptic target cells. A basket cell inn ervated a pyramidal cell via fifteen release sites; the numbers of syn apses formed by three dendrite-targeting cells on pyramidal cells were seventeen and eight respectively, and three on a spiny stellate cell; the interaction between a double bouquet cell and a postsynaptic pyra midal cell was mediated by ten synaptic junctions. 5. All three types of interneurone (n = 6; 2 for each type of cell) elicited short-latenc y IPSPs with fast rise time (10-90%; 2.59 +/- 1.02 ms) and short durat ion (at half-amplitude, 15.82 +/- 5.24 ms), similar to those mediated by GABA(A) receptors. 6. Average amplitudes of unitary IPSPs (n = 6) w ere 845 +/- 796 mu V (range, 134-2265 mu V). Variability of IPSP ampli tude was moderate, the average ratio of IPSP and baseline noise varian ce was 1.54 +/- 0.96. High frequency activation of single presynaptic dendrite-targeting cells led to an initial summation followed by use-d ependent depression of the averaged postsynaptic response. Double bouq uet cell-evoked IPSPs, recorded in the soma, had a smaller amplitude t han those evoked by the other two cell types. In all connections, tran smission failures were rare or absent, particularly when mediated by a high number of release sites. 7. The results demonstrate that differe nt types of neocortical GABAergic neurones innervate distinct domains on the surface of their postsynaptic target cells. Nevertheless, all t hree types of cell studied here elicit fast IPSPs and provide GABAergi c input through multiple synaptic release sites with few, if any, fail ures of transmission.