Song recognition learning and stimulus-specific weakening of neural responses in the avian auditory forebrain

Learning typically increases the strength of responses and the number of neurons that respond to training stimuli. Few studies have explored representational plasticity using natural stimuli, however, leaving unknown the changes that accompany learning under more realistic conditions. Here, we examine experience-dependent plasticity in European starlings, a songbird with rich acoustic communication signals tied to robust, natural recognition behaviors. We trained starlings to recognize conspecific songs and recorded the extracellular spiking activity of single neurons in the caudomedial nidopallium (NCM), a secondary auditory forebrain region analogous to mammalian auditory cortex. Training induced a stimulus-specific weakening of the neural responses (lower spike rates) to the learned songs, whereas the population continued to respond robustly to unfamiliar songs. Additional experiments rule out stimulus-specific adaptation and general biases for novel stimuli as explanations of these effects. Instead, the results indicate that associative learning leads to single neuron responses in which both irrelevant and unfamiliar stimuli elicit more robust responses than behaviorally relevant natural stimuli. Detailed analyses of these effects at a finer temporal scale point to changes in the number of motifs eliciting excitatory responses above a neuron's spontaneous discharge rate. These results show a novel form of experience-dependent plasticity in the auditory forebrain that is tied to associative learning and in which the overall strength of responses is inversely related to learned behavioral significance.