Lateral interactions at direction-selective striate neurones in the cat demonstrated by local cortical inactivation.

Abstract

1. Single neurones were recorded with glass-coated tungsten electrodes from area 17 of the cat's visual cortex. The cats were anaesthetized and artificially respirated with a mixture of halothane, nitrous oxide and oxygen. 2. For local cortical inactivation a multibarrel pipette was placed 0.5-2.5 mm posterior (or anterior) to the recording site, at a depth of 400-600 micron. Four separate barrels of the pipette were filled with gamma-aminobutyric acid (GABA); the fifth was filled with Pontamine Sky Blue for labelling of the centre of the inactivation site. 3. Direction-selective cells, of differing optimal orientations and preferred directions of motion, were classified as simple or complex and tested with computer-controlled stimuli presented on an oscilloscope. 4. During continuous recording GABA was microionophoretically applied for different durations and with different ejection currents. The effectiveness of GABA microionophoresis was evident from the direct GABAergic effects (strong overall inhibition of the recorded cells) observed with high ejection currents and prolonged application. 5. Two discrete effects could be observed during local inactivation distant from the cortical cell under study: an increase of the response in either the non-preferred or the preferred direction; or a decrease of the response in the preferred direction. All GABA-induced changes were reversible. 6. The depressant action of GABA was independent of the relative topography between recording and inactivation site and affected mainly the response to the preferred direction of stimulus motion. 7. Disinhibition was only observed when the stimulus-evoked response moved on the cortical map in a direction from the GABA pipette towards the recording electrode. It is concluded that GABA reversibly silences inhibitory interneurones that are situated in the vicinity of the micropipette tip and are involved in generation of direction selectivity. 8. No fundamental differences between cells from different cortical layers were observed. The disinhibitory effects of GABA inactivation were more pronounced and more frequently seen in simple cells (61%) than in complex cells (38%), while the opposite was true for reduced excitation during lateral GABA inactivation (observed in 62% of the complex vs. 39% of the simple cells). Accordingly, lateral inhibition statistically prevails in simple cells and lateral excitation in complex cells. 9. Among the inhibitory and excitatory mechanisms affected by lateral GABA inactivation, inhibition is organized with a higher topographic specificity.