Tone-Specific and Nonspecific Plasticity of Inferior Colliculus Elicited by Pseudo-Conditioning: Role of Acetylcholine and Auditory and Somatosensory Cortices

Experience-dependent plasticity in the central sensory systems depends on activation of both the sensory and neuromodulatory systems. Sensitization or nonspecific augmentation of central auditory neurons elicited by pseudo-conditioning with unpaired conditioning tonal (CS) and unconditioned electric leg (US) stimuli is quite different from tone-specific plasticity, called best frequency (BF) shifts, of the neurons elicited by auditory fear conditioning with paired CS and US. Therefore the neural circuits eliciting the nonspecific augmentation must be different from that eliciting the BF shifts. We first examined plastic changes in the response properties of collicular neurons of the big brown bat elicited by pseudo-conditioning and found that it elicited prominent nonspecific augmentation-an auditory response increase, a frequency-tuning broadening, and a threshold decreas-and that, in addition, it elicited a small short-lasting BF shift only when the CS frequency was 5 kHz lower than the BF of a recorded neuron. We examined the role of acetylcholine and the auditory and somatosensory cortices in these collicular changes. The development of the nonspecific augmentation was affected little by a muscarinic acetylcholine receptor antagonist applied to the inferior colliculus and by a GABA(A) receptor agonist applied to the auditory or somatosensory cortex. However, these drugs abolished the small short-lasting BF shift as they abolished the large long-lasting cortical and short-lasting collicular BF shifts elicited by the conditioning. These results indicate that, different from the BF shift, the nonspecific augmentation of the inferior colliculus depends on neither the cholinergic neuromodulator nor the auditory and somatosensory cortices.