Neural mechanisms for sparse, informative and background-invariant coding of vocalizations

To efficiently process natural environments, many species have sensory systems that selectively encode behaviorally relevant information. Vocal communicators such as humans and songbirds rely on their auditory systems to recognize vocalizations and to extract vocalizations from complex auditory scenes. Yet many of the neural correlates of these perceptual abilities remain poorly understood. In this dissertation, I describe neural mechanisms by which the songbird auditory system produces sparse, informative and background-invariant neural representations of vocalizations. First, I show that auditory midbrain neurons encode vocalizations differently than other complex sounds, and that subthreshold excitation and inhibition may facilitate stimulus-dependent encoding of vocalizations. Second, I show that the responses of individual midbrain neurons can be unreliable, and that pooling the responses of correlated and similarly tuned neurons facilitates the neural discrimination of vocalizations. Third, I show that sparse coding neurons in the songbird forebrain extract individual vocalizations from auditory scenes at signal-to-noise ratios that match behavior. Lastly, I show that a simple neural circuit of delayed inhibition transforms a dense and background-sensitive neural representation into a sparse and background-invariant representation, in as little as one synapse. Together, these findings illuminate previously unknown mechanisms for selective vocalization coding, suggest a behaviorally relevant role for the ubiquitous phenomenon of sparse neural coding, and provide a neural correlate for the perceptual extraction of vocalizations from complex auditory scenes

Influences of behavioral state and developmental vocal learning on neural coding in the songbird auditory system

Vocal communicators such as humans and songbirds rely on their auditory systems to learn, recognize, and encode acoustic features of communication vocalizations. Yet it remains unclear how varying behavioral, experimental, and developmental contexts impact neural coding in the songbird auditory system. In this dissertation I demonstrate that experimental and behavioral contexts relating to arousal are sufficient to alter neural excitability in a way that has implications for neural coding in the songbird auditory system. First I show that urethane, a common anesthetic used in neurophysiological studies of songbird and mammalian auditory neurons, suppresses neural excitability but does not alter spectrotemporal tuning or neural discrimination in single auditory midbrain neurons. Next, I demonstrate that neurons in the songbird primary auditory cortical region Field L are sensitive to local concentrations of norepinephrine, a neurotransmitter involved mediating changes in arousal and behavioral state. Lastly, I report the results of a developmental study that demonstrates experience-dependent changes in temporal and spectral tuning in songbird auditory cortical neurons during vocal learning. These developmental effects were found to have region and cell-type specificity, and highlight potential functional roles for dorsal and ventral auditory cortical neurons in the songbird auditory cortex. The findings reported here have important implications for future studies into the neurophysiology of vocal learning

Seeing sound: a new way to illustrate auditory objects and their neural correlates

This thesis develops a new method for time-frequency signal processing and examines the relevance of the new representation in studies of neural coding in songbirds. The method groups together associated regions of the time-frequency plane into objects defined by time-frequency contours. By combining information about structurally stable contour shapes over multiple time-scales and angles, a signal decomposition is produced that distributes resolution adaptively. As a result, distinct signal components are represented in their own most parsimonious forms.  Next, through neural recordings in singing birds, it was found that activity in song premotor cortex is significantly correlated with the objects defined by this new representation of sound. In this process, an automated way of finding sub-syllable acoustic transitions in birdsongs was first developed, and then increased spiking probability was found at the boundaries of these acoustic transitions. Finally, a new approach to study auditory cortical sequence processing more generally is proposed. In this approach, songbirds were trained to discriminate Morse-code-like sequences of clicks, and the neural correlates of this behavior were examined in primary and secondary auditory cortex. It was found that a distinct transformation of auditory responses to the sequences of clicks exists as information transferred from primary to secondary auditory areas. Neurons in secondary auditory areas respond asynchronously and selectively -- in a manner that depends on the temporal context of the click. This transformation from a temporal to a spatial representation of sound provides a possible basis for the songbird's natural ability to discriminate complex temporal sequences

Neural processing of natural sounds

Natural sounds include animal vocalizations, environmental sounds such as wind, water and fire noises and non-vocal sounds made by animals and humans for communication. These natural sounds have characteristic statistical properties that make them perceptually salient and that drive auditory neurons in optimal regimes for information transmission.Recent advances in statistics and computer sciences have allowed neuro-physiologists to extract the stimulus-response function of complex auditory neurons from responses to natural sounds. These studies have shown a hierarchical processing that leads to the neural detection of progressively more complex natural sound features and have demonstrated the importance of the acoustical and behavioral contexts for the neural responses.High-level auditory neurons have shown to be exquisitely selective for conspecific calls. This fine selectivity could play an important role for species recognition, for vocal learning in songbirds and, in the case of the bats, for the processing of the sounds used in echolocation. Research that investigates how communication sounds are categorized into behaviorally meaningful groups (e.g. call types in animals, words in human speech) remains in its infancy.Animals and humans also excel at separating communication sounds from each other and from background noise. Neurons that detect communication calls in noise have been found but the neural computations involved in sound source separation and natural auditory scene analysis remain overall poorly understood. Thus, future auditory research will have to focus not only on how natural sounds are processed by the auditory system but also on the computations that allow for this processing to occur in natural listening situations.The complexity of the computations needed in the natural hearing task might require a high-dimensional representation provided by ensemble of neurons and the use of natural sounds might be the best solution for understanding the ensemble neural code

Behavioral and neural selectivity for acoustic signatures of vocalizations

Vocal communication relies on the ability of listeners to identify, process, and respond to vocal sounds produced by others in complex environments. In order to accurately recognize these signals, animals’ auditory systems must robustly represent acoustic features that distinguish vocal sounds from other environmental sounds. In this dissertation, I describe experiments combining acoustic, behavioral, and neurophysiological approaches to identify behaviorally relevant vocalization features and understand how they are represented in the brain. First, I show that vocal responses to communication sounds in songbirds depend on the presence of specific spectral signatures of vocalizations. Second, I identify an anatomically localized neural population in the auditory cortex that shows selective responses for behaviorally relevant sounds. Third, I show that these neurons’ spectral selectivity is robust to acoustic context, indicating that they could function as spectral signature detectors in a variety of listening conditions. Last, I deconstruct neural selectivity for behaviorally relevant sounds and show that it is driven by a sensitivity to deep fluctuations in power along the sound frequency spectrum. Together, these results show that the processing of behaviorally relevant spectral features engages a specialized neural population in the auditory cortex, and elucidate an acoustic driver of vocalization selectivity

Subdivisions of the Auditory Midbrain (N. Mesencephalicus Lateralis, pars dorsalis) in Zebra Finches Using Calcium-Binding Protein Immunocytochemistry

The midbrain nucleus mesencephalicus lateralis pars dorsalis (MLd) is thought to be the avian homologue of the central nucleus of the mammalian inferior colliculus. As such, it is a major relay in the ascending auditory pathway of all birds and in songbirds mediates the auditory feedback necessary for the learning and maintenance of song. To clarify the organization of MLd, we applied three calcium binding protein antibodies to tissue sections from the brains of adult male and female zebra finches. The staining patterns resulting from the application of parvalbumin, calbindin and calretinin antibodies differed from each other and in different parts of the nucleus. Parvalbumin-like immunoreactivity was distributed throughout the whole nucleus, as defined by the totality of the terminations of brainstem auditory afferents; in other words parvalbumin-like immunoreactivity defines the boundaries of MLd. Staining patterns of parvalbumin, calbindin and calretinin defined two regions of MLd: inner (MLd.I) and outer (MLd.O). MLd.O largely surrounds MLd.I and is distinct from the surrounding intercollicular nucleus. Unlike the case in some non-songbirds, however, the two MLd regions do not correspond to the terminal zones of the projections of the brainstem auditory nuclei angularis and laminaris, which have been found to overlap substantially throughout the nucleus in zebra finches

Cortical And Subcortical Mechanisms For Sound Processing

The auditory cortex is essential for encoding complex and behaviorally relevant sounds. Many questions remain concerning whether and how distinct cortical neuronal subtypes shape and encode both simple and complex sound properties. In chapter 2, we tested how neurons in the auditory cortex encode water-like sounds perceived as natural by human listeners, but that we could precisely parametrize. The stimuli exhibit scale-invariant statistics, specifically temporal modulation within spectral bands scaled with the center frequency of the band. We used chronically implanted tetrodes to record neuronal spiking in rat primary auditory cortex during exposure to our custom stimuli at different rates and cycle-decay constants. We found that, although neurons exhibited selectivity for subsets of stimuli with specific statistics, over the population responses were stable. These results contribute to our understanding of how auditory cortex processes natural sound statistics. In chapter 3, we review studies examining the role of different cortical inhibitory interneurons in shaping sound responses in auditory cortex. We identify the findings that support each other and the mechanisms that remain unexplored. In chapter 4, we tested how direct feedback from auditory cortex to the inferior colliculus modulated sound responses in the inferior colliculus. We optogenetically activated or suppressed cortico-collicular feedback while recording neuronal spiking in the mouse inferior colliculus in response to pure tones and dynamic random chords. We found that feedback modulated sound responses by reducing sound selectivity by decreasing responsiveness to preferred frequencies and increasing responsiveness to less preferred frequencies. Furthermore, we tested the effects of perturbing intra-cortical inhibitory-excitatory networks on sound responses in the inferior colliculus. We optogenetically activated or suppressed parvalbumin-positive (PV) and somatostatin-positive (SOM) interneurons while recording neuronal spiking in mouse auditory cortex and inferior colliculus. We found that modulation of neither PV- nor SOM-interneurons affected sound-evoked responses in the inferior colliculus, despite significant modulation of cortical responses. Our findings imply that cortico-collicular feedback can modulate responses to simple and complex auditory stimuli independently of cortical inhibitory interneurons. These experiments elucidate the role of descending auditory feedback in shaping sound responses. Together these results implicate the importance of the auditory cortex in sound processing

Linear and Nonlinear Auditory Response Properties Of Interneurons In A High Order Avian Vocal Motor Nucleus During Wakefulness

Motor-related forebrain areas in higher vertebrates also show responses to passively presented sensory stimuli. Sensory tuning properties in these areas, especially during wakefulness, and their relation to perception, however, are poorly understood. In the avian song system, HVC (proper name) is a vocal-motor structure with auditory responses well defined under anesthesia but poorly characterized during wakefulness. I used a large set of song stimuli including the bird‟s own song (BOS) and many conspecific stimuli (CON) to characterize auditory tuning properties in putative interneurons (HVCIN) during wakefulness. My findings suggest that HVC contains a heterogeneity of response types; a third of neurons are either suppressed or show no response to any stimuli and two thirds show excitatory responses to one or more stimuli. A subset of excitatory neurons are tuned exclusively to BOS and show very low linearity as measured by spectrotemporal receptive field analysis (STRF), but many respond well to both BOS and CON stimuli and show response linearity comparable to that previously measured in structures of the ascending auditory pathway. Fourier analysis of the STRFs of linear HVCIN reveals a range of peak spectrotemporal tuning properties, with approximately half of these neurons showing peak sensitivity to modulations occurring with high power in zebra finch song. Previous work has established that HVC lesioned birds are impaired in operant contingency reversals involving CON stimuli and birds with lesions to song nuclei receiving auditory input from HVC are impaired in discriminations between BOS and CON stimuli. The findings of the present study are consistent with these results and suggest a possible role for HVC in species-relevant auditory tasks