Dissection of the neuron network in the catfish inner retina. IV. Bidirectional interactions between amacrine and ganglion cells.

1. We have functionally dissected the neuron network in the catfish inner retina by means of current injection. Simultaneous intracellular recordings were made from two neighboring neurons with the use of two separate electrodes. Extrinsic current was injected into one neuron, and the resulting intracellular responses were recorded from the other neuron. The test signals included 1) a single-frequency sinusoid, 2) a depolarizing or a hyperpolarizing current pulse, and 3) white-noise modulated current from which Wiener kernels were computed by an input-output cross-correlation process. 2. Extrinsic current injected into an ON amacrine (NA) cell evoked responses from a neighboring ON ganglion (GA) cell. Conversely, current injected into a GA cell elicited responses from a neighboring NA cell. Similar results were obtained for the transmission between OFF amacrine (NB) and OFF ganglion (GB) cells. Neural filters for the forward and backward transmissions between amacrine and ganglion cells of the same response polarity were low-pass, constant gain with a cutoff frequency of 40-50 Hz. The gain measured by current-amplitude relationships was comparable for the forward (N----G) and backward (G----N) transmission. 3. Similar bidirectional signal transmission was found between amacrine cells and between ganglion cells of the same response polarity. Neural filters for such transmission were also low-pass, constant gain with a cutoff frequency of 40-50 Hz. 4. Because a large portion of the current-evoked response was predicted by the first-order kernel, transmission between cells of the same response polarity was approximately linear. The current-evoked first-order kernels were brief and impulse-like compared with the light-evoked first-order kernels. 5. We conclude that ON and OFF amacrine and ganglion cells form two ON- and OFF-cell clusters in which cells are extensively and bidirectionally interconnected, enhancing the response in each cluster.