Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons

Abstract Intensity-tuned auditory cortex neurons have spike rates that are nonmonotonic functions of sound intensity: their spike rate initially increases and peaks as sound intensity is increased, then decreases as sound intensity is further increased. They are either “unbalanced,” receiving disproportionally large synaptic inhibition at high sound intensities; or “balanced,” receiving intensity-tuned synaptic excitation and identically tuned synaptic inhibition which neither creates enhances nor creates intensity-tuning. It has remained unknown if the synaptic inhibition received by unbalanced neurons enhances intensity-tuning already present in the synaptic excitation, or if it creates intensity-tuning that is not present in the synaptic excitation. Here we show, using in vivo whole cell recordings in pentobarbital-anesthetized rats, that in some unbalanced intensity-tuned auditory cortex neurons synaptic inhibition enhances the intensity-tuning; while in others it actually creates the intensity-tuning. The lack of balance between synaptic excitation and inhibition was not always apparent in their peak amplitudes, but could sometimes be revealed only by considering their relative timing. Since synaptic inhibition is essentially cortical in origin, the unbalanced neurons in which inhibition creates intensity-tuning provide examples of auditory feature-selectivity arising de novo at the auditory cortex.