Orientation-sensitive amacrine and ganglion cells in the rabbit retina

1. Intracellular recordings were obtained from amacrine and ganglion cells in the isolated, superfused retina-eyecup preparation of the rabbit to test the orientation sensitivity of their responses. Cell identification was based on morphological criteria following injection of horseradish peroxidase (HRP) or N-(2-aminoethyl)-biotinamide hydrochloride (Neurobiotin) to visualize soma-dendritic architectures. 2. In terms of the physiological mechanisms generating their sensitivity, two types of orientation-sensitive amacrine cell and a single type of orientation-sensitive ganglion cell were found. These cell types were termed orientation selective and orientation biased. Cells were subtypes further into on- or off-center receptive-field categories. 3. The receptive fields of orientation-selective amacrine and ganglion cells were composed of two inhibitory fields that flanked the excitatory center receptive field along the preferred orientation. These inhibitory flanks produced a center receptive-field anisotropy with its major axis corresponding to the preferred orientation: either parallel or orthogonal to the visual streak. When a stimulus was oriented orthogonal to the preferred orientation (i.e., at the null orientation), the inhibitory fields were stimulated, resulting in a null inhibition that blocked the center-mediated excitation. Stimulation of these inhibitory flanks was absolutely essential to evoke the orientation selectivity of these cells. The null response reflected inhibition associated with a conductance increase and not disfacilitation. 4. Orientation-biased amacrine cells displayed a center receptive-field anisotropy with its major axis oriented either parallel or orthogonal to the visual streak. These cells preferred light stimuli oriented along the major axis of the center receptive field. However, whereas the excitatory response of these cells was reduced when a stimulus was rotated from the preferred orientation, there was no corresponding hyperpolarization. No null inhibition was detected even after modulation of the membrane potential with extrinsic current. 5. Although orientation-biased amacrine cells were morphologically heterogeneous, they all displayed dendritic arbors that were markedly elongated along an axis corresponding to their physiological preferred orientation. Thus it appears that the elongated dendritic fields of these cells may provide for the anisotropy of their center receptive fields and, in turn, their orientation sensitivity. 6. Orientation-selective amacrine cells formed a rather homogeneous morphological group of cells. These neurons displayed large, radially symmetric dendritic arbors with diameters averaging 1,100 microns. There were no asymmetries in their dendritic fields and thus no clear structural basis for their orientation selectivity. 7. In contrast, orientation-selective ganglion cells displayed diverse soma-dendritic architecture and thus could not be placed into a single morphological class.(ABSTRACT TRUNCATED AT 400 WORDS)