Physiological correspondence dictates cortical long-term potentiation and depression by thalamic induction

The auditory cortex exhibits frequency-specific plasticity over a life cycle. Although thalamocortical long-term potentiation (LTP) and depression (LTD) are components of a widely held model underlying the receptive field (RF) plasticity of cortical neurons, the model lacks direct supporting evidence. We show here that conventional high-frequency tetanic stimulation (TS) of the auditory thalamus induced long-term changes in cortical field excitatory postsynaptic potentials, including both LTP and LTD, in mice. Thalamic TS induced LTP when the stimulated thalamic and recorded cortical neurons were tuned to the same frequency and induced LTD when they were tuned to different frequencies. The thalamocortical LTP was N-methyl-d-aspartate-dependent, but the LTD also involved cortical γ-amino-butyric acidergic inhibition. Notably, the frequency-specificity of cortical LTP/LTD was in accordance with the frequency-specific plasticity of spike-based RFs of cortical neurons. Our results suggest that cortical LTP and LTD induced by thalamic induction can be a consequence of identical stimuli, occur in an input-specific manner, and account for frequency-specific remodeling of RFs of auditory cortical neurons.