Stimulus-Dependent Auditory Tuning Results in Synchronous Population Coding of Vocalizations in the Songbird Midbrain

Abstract

Physiological studies in vocal animals such as songbirds indicate that vocalizations drive auditory neurons particularly well. But the neural mechanisms whereby vocalizations are encoded differently from other sounds in the auditory system are unknown. We used spectrotemporal receptive fields (STRFs) to study the neural encoding of song versus the encoding of a generic sound, modulationlimited noise, by single neurons and the neuronal population in the zebra finch auditory midbrain. The noise was designed to match song in frequency, spectrotemporal modulation boundaries, and power. STRF calculations were balanced between the two stimulus types by forcing a common stimulus subspace. We found that 91% of midbrain neurons showed significant differences in spectral and temporal tuning properties when birds heard song and when birds heard modulation-limited noise. During the processing of noise, spectrotemporal tuning was highly variable across cells. During song processing, the tuning of individual cells became more similar; frequency tuning bandwidth increased, best temporal modulation frequency increased, and spike timing became more precise. The outcome was a population response to song that encoded rapidly changing sounds with power and precision, resulting in a faithful neural representation of the temporal pattern of a song. Modeling responses to song using the tuning to modulation-limited noise showed that the population response would not encode song as precisely or robustly. We conclude that stimulus-dependent changes in auditory tuning during song processing facilitate the high-fidelity encoding of the temporal pattern of a song.

Hemispheric differences in processing of vocalizations depend on early experience

“…The lateral asymmetries suggest that conspecific vocalizations either engage different network properties in each hemisphere or trigger a gating process that routes information differentially to each hemisphere. With respect to the latter possibility, it has been suggested that asymmetrical inhibitory influences in the brainstem auditory system may contribute to lateral differences in the mammalian cortex (17) and that sound context changes tuning functions in the brainstem auditory system of a songbird (18). However, neither the mechanism nor the functional meaning of the lateral differences in ARM's and adaptation rates can be determined from the present experiments.…”

Differential Influence of Frequency, Timing, and Intensity Cues in a Complex Acoustic Categorization Task

“…Many neurons in field L, the avian analog of primary auditory cortex, are tightly tuned in time (Nagel and Doupe 2008), causing them to respond to syllable onsets with precisely time-locked spikes (Woolley et al 2006). This temporal pattern of spiking provides significant information about what song was heard (Narayan et al 2006), and several papers have therefore suggested that these temporal patterns of spiking are critical for birds' discrimination and recognition of songs (Larson et al 2009;Wang et al 2007).…”

“…The neural representation of songs-particularly in the primary auditory area field L Margoliash 1992, 1995;Vates et al 1996)-has been studied in detail Doupe 2006, 2008;Narayan et al 2006;Sen et al 2001;Theunissen et al 2000;Wang et al 2007;Woolley et al 2005Woolley et al , 2006Woolley et al , 2009. Most field L neurons are highly tuned in frequency, time, or both (Nagel and Doupe 2008;Woolley et al 2009).…”

Spatial structure of neuronal receptive field in awake monkey secondary visual cortex (V2)

“…We then turned to the modified spike-triggered average or spike-triggered covariance (mSTA/STC) method for comparison with PPR. The mSTA/STC analysis for natural stimuli have been described previously (21,(56)(57)(58). For comparison, we constructed the RF models by mSTA/STC with the same number of subunits as those from PPR for each cell.…”