Modulation Power and Phase Spectrum of Natural Sounds Enhance Neural Encoding Performed by Single Auditory Neurons

Abstract

We examined the neural encoding of synthetic and natural sounds by single neurons in the auditory system of male zebra finches by estimating the mutual information in the time-varying mean firing rate of the neuronal response. Using a novel parametric method for estimating mutual information with limited data, we tested the hypothesis that song and song-like synthetic sounds would be preferentially encoded relative to other complex, but non-song-like synthetic sounds. To test this hypothesis, we designed two synthetic stimuli: synthetic songs that matched the power of spectral-temporal modulations but lacked the modulation phase structure of zebra finch song and noise with uniform band-limited spectral-temporal modulations. By defining neural selectivity as relative mutual information, we found that the auditory system of songbirds showed selectivity for song-like sounds. This selectivity increased in a hierarchical manner along ascending processing stages in the auditory system. Midbrain neurons responded with highest information rates and efficiency to synthetic songs and thus were selective for the spectral-temporal modulations of song. Primary forebrain neurons showed increased information to zebra finch song and synthetic song equally over noise stimuli. Secondary forebrain neurons responded with the highest information to zebra finch song relative to other stimuli and thus were selective for its specific modulation phase relationships. We also assessed the relative contribution of three response properties to this selectivity: (1) spiking reliability, (2) rate distribution entropy, and (3) bandwidth. We found that rate distribution and bandwidth but not reliability were responsible for the higher average information rates found for song-like sounds.

Distinct Time Scales in Cortical Discrimination of Natural Sounds in Songbirds

“…Yet to our knowledge, only one previous study has examined neural discrimination of complex sounds based on the average cortical population activity in primary auditory cortex (Orduña et al 2005). In songbirds, previous studies at the cortical level have quantified information transmitted by single neurons (Hsu et al 2004;Wright et al 2002), discriminability between different categories of natural and synthetic sounds based on mean firing rates (Amin et al 2004;Grace et al 2003), and discriminability between different categories of natural sounds by ensembles of neurons (Woolley et al 2005). This is the first study to quantify the contribution of spike timing to the discrimination of complex sounds by single neurons at the cortical level and the time scales underlying such discrimination.…”

Probabilistic Encoding of Vocalizations in Macaque Ventral Lateral Prefrontal Cortex

“…They were subsequently filtered using a symmetric two-dimensional (2D) Gaussian window with an SD of 1.3 samples. Modulation spectra were then calculated by taking the 2D Fourier transform of the spectrogram, and computing its power (Singh et al, 2003;Hsu et al, 2004). The average frequency modulation was then calculated by averaging along the temporal axis of the modulation spectra, and the average temporal modulation was calculated by averaging along the frequency axis.…”

“…Although representations close to sensory receptors can be reasonably well characterized by models that assume the responses are linearly related to simple features of the stimuli (Kim and Young, 1994;Pillow et al, 2005), these models fail as early as the cochlear nucleus (Nelken et al, 1997) and the inferior colliculus (Escabi and Schreiner, 2002) in the auditory system. Many laboratories are investigating the special problems associated with natural stimuli and sensory systems (Theunissen et al, 2000;Vinje and Gallant, 2000;Hsu et al, 2004;Machens et al, 2004). An ecologically important class of natural stimuli for primates is their vocalizations Hauser, 1999, 2001;Seyfarth et al, 2005), and an extensive body of behavioral research has shown that primates, including rhesus macaques, discriminate among different calls (Dittus, 1984;Gouzoules et al, 1984;Cheney and Seyfarth, 1988;Gouzoules et al, 1998).…”

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

“…These areas are likely to be modulated by experience and learning. Indeed, unit recordings show that neuronal responses are more selectively tuned to learned vocal sounds in NCM (20,21) and CM (43)(44)(45), whereas the primary auditory subregions L2a and L2b are responsive to sounds within the wider species-specific spectrotemporal range (24,46,47). Measurement of long-term response habituation in NCM, by both electrophysiology and the study of the song stimulation-induced up-regulation of ZENK, has suggested that this area might encode the long-lasting sensory memory of the TUT (31,40).…”