Representations of conspecific song by starling secondary forebrain auditory neurons: toward a hierarchical framework

The functional organization giving rise to stimulus selectivity in higher-order auditory neurons remains under active study. We explored the selectivity for motifs, spectrotemporally distinct perceptual units in starling song, recording the responses of 96 caudomedial mesopallium (CMM) neurons in European starlings (Sturnus vulgaris) under awake-restrained and urethane-anesthetized conditions. A subset of neurons was highly selective between motifs. Selectivity was correlated with low spontaneous firing rates and high spike timing precision, and all but one of the selective neurons had similar spike waveforms. Neurons were further tested with stimuli in which the notes comprising the motifs were manipulated. Responses to most of the isolated notes were similar in amplitude, duration, and temporal pattern to the responses elicited by those notes in the context of the motif. For these neurons, we could accurately predict the responses to motifs from the sum of the responses to notes. Some notes were suppressed by the motif context, such that removing other notes from motifs unmasked additional excitation. Models of linear summation of note responses consistently outperformed spectrotemporal receptive field models in predicting responses to song stimuli. Tests with randomized sequences of notes confirmed the predictive power of these models. Whole notes gave better predictions than did note fragments. Thus in CMM, auditory objects (motifs) can be represented by a linear combination of excitation and suppression elicited by the note components of the object. We hypothesize that the receptive fields arise from selective convergence by inputs responding to specific spectrotemporal features of starling notes.