Optical imaging of spatiotemporal patterns of glutamatergic excitation and GABAergic inhibition in the guinea-pig auditory cortex in vivo.

1. Glutamatergic excitation and gamma-aminobutyric acid (GABA)-ergic inhibition in layers II and III of the auditory cortex of anaesthetized guinea-pigs were recorded optically using a voltage-sensitive dye RH795 and a 12 x 12 photodiode array. 2. After contralateral ear stimulation with pure tones, transient excitatory responses followed by inhibitory responses were observed in fields A (primary) and DC of the auditory cortex. The area of the excitatory responses was sandwiched or surrounded by the areas of the inhibitory responses. 3. Optically recorded excitatory responses to pure tones had two components: a component sensitive to 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), a non-N-methyl-D-aspartate (non-NMDA) receptor antagonist, and a component sensitive to 2-amino-5-phosphono-valerate (APV), an NMDA receptor antagonist. Application of CNQX (5 microM) to the auditory cortex suppressed an early, but not a late, phase of the excitation; application of APV (100 microM) had the opposite effect. Concomitant application of CNQX and bicuculline methiodide (BMI, 4 microM), a GABAA receptor antagonist, increased the amplitude of the late phase 4-fold. This enhanced response was suppressed by APV. 4. These results indicate that (i) auditory cortical excitatory responses are mediated by both non-NMDA and NMDA receptors, (ii) inhibition is mediated by GABAA receptors, (ii) the excitatory bands are sandwiched or surrounded by GABAA receptor-mediated inhibitory areas and (iv) GABAA receptors effectively inhibit the NMDA, but not the non-NMDA, receptor-mediated excitation.