Synapses of optic axons with GABA- and glutamate-containing elements in the optic tectum of Bufo marinus

The central termination and the transmitter content of the optic fibers and the neurochemical nature of their synaptic targets was investigated in the optic tectum of the toad Bufo marinus. Retinal ganglion cells were retrogradely filled from the tectum with the fluorescent dye DiI and the retinal wholemounts were immunostained for glutamate. Most of the dye-filled cells could be double labeled. In addition, double-labeling for gamma-aminobutyric acid an glutamate were also made, when colocalization of these markers was not observed in the neurons of the retinal ganglion cell layer. In order to identify retinal terminals in the optic tectum, optic axons were retrogradely filled with horseradish peroxidase. Postembedding immunocytochemistry showed that 88% of the optic axon terminals were glutamate-like immunoreactive, 6% gamma-aminobutyric acid-immunoreactive and 6% were negative for both GABA and glutamate. Optic fibre terminals synapsed on gamma-aminobutyric acid- or glutamate-containing postsynaptic profiles (58% and 7%, respectively), while the rest on immunonegative elements. Optic fibres containing glutamate rarely synapsed with glutamate-like immunoreactive postsynaptic elements. In contrast, 67% of the gamma-aminobutyric acid-immunoreactive optic terminals synapsed onto gamma-aminobutyric acid-positive dendrites. It has been observed after combination of anterograde tracer transport and double-label immunocytochemistry, that 57% of the optic terminals synapsed on gamma-aminobutyric acid-immunoreactive elements and 38% on dendrites containing neither gamma-aminobutyric acid- nor glutamate-immunoreactive materials. These results suggest that (1) a large number of ganglion cells use glutamate and some gamma-aminobutyric acid as a transmitter, (2) a substantial proportion of the optic axons terminate on gamma-aminobutyric acid-containing inhibitory interneurons in the tectum, (3) some intrinsic neurons in the tectum are glutamate-like immunoreactive. We also propose, that (4) gamma-aminobutyric acid-immunoreactive optic axons may form an effective disinhibitory circuit in the tectum by synapsing preferentially with local inhibitory interneurons.