Global evaluation of contributions of GABAA, AMPA and NMDA receptors to orientation maps in cat's visual cortex

Orientation selectivity is a fundamental property of neurons in the visual cortex for form perception. Cortical cells with similar preferred orientations are organized in a columnar manner to form a two-dimensional orientation map in the primary visual cortex (area 17). There are several mechanisms underlying the generation of orientation selectivity at the single neuron level; however, their relative contributions to the overall orientation maps are unclear. Using optical imaging combined with in vivo application of AMPA, NMDA and GABAA receptor antagonists, we observed that CNQX or AP-5 weakened the orientation map of area 17, whereas simultaneous application of both antagonists abolished the map completely. Furthermore, removal of GABAergic inhibition by application of bicuculline and/or picrotoxin, which are GABAA receptor antagonists, led to cortical epilepsy and wiped out the orientation map completely; although low doses of bicuculline enhanced the orientation map. The orientation map reappeared after the bicuculline-induced epilepsy was prevented by applying CNQX to partially block the excitatory inputs. During those drug application experiments that did not abolish orientation selectivity, the remained map pattern was unchanged. Bicuculline combined with CNQX could only reduce the amplitude of orientation mapping signals but could not alter the preferred orientation maps. These results indicate that the excitatory inputs to cortical neurons are essential and sufficient for generating orientation maps. However, intracortical GABAergic inhibition is necessary to sustain a normal excitation-inhibition balance in area 17. Overall, both excitatory and inhibitory inputs have spatially homogenous impact on orientation maps.