Imaging Learned Song Representations in Populations of Sensorimotor Neurons Essential to Vocal Communication

Perceiving or producing complex vocalizations such as speech and birdsongs require the coordinated activity of neuronal populations, and these activity patterns can vary over space and time. How learned communication signals are represented by populations of sensorimotor neurons essential to vocal perception and production remains poorly understood. Using a combination of two-photon calcium imaging, intracellular electrophysiological recording and retrograde tracing methods in anesthetized adult male zebra finches (Taeniopygia guttata), I addressed how the bird's own song and its component syllables are represented by the spatiotemporal patterns of activity of two spatially intermingled populations of projection neurons (PNs) in HVC, a sensorimotor area required for song perception and production. These experiments revealed that neighboring PNs can respond at markedly different times to song playback and that different syllables activate spatially intermingled HVC PNs within a small region. Moreover, noise correlation analysis reveals enhanced functional connectivity between PNs that respond most strongly to the same syllable and also provides evidence of a spatial gradient of functional connectivity specific to PNs that project to song motor nucleus (i.e. HVC_RA cells). These findings support a model in which syllabic and temporal features of song are represented by spatially intermingled PNs functionally organized into cell- and syllable-type networks.

Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds.

Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other's pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.

Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds.

Mechanisms for the evolution of convergent behavioral traits are largely unknown. Vocal learning is one such trait that evolved multiple times and is necessary in humans for the acquisition of spoken language. Among birds, vocal learning is evolved in songbirds, parrots, and hummingbirds. Each time similar forebrain song nuclei specialized for vocal learning and production have evolved. This finding led to the hypothesis that the behavioral and neuroanatomical convergences for vocal learning could be associated with molecular convergence. We previously found that the neural activity-induced gene dual specificity phosphatase 1 (dusp1) was up-regulated in non-vocal circuits, specifically in sensory-input neurons of the thalamus and telencephalon; however, dusp1 was not up-regulated in higher order sensory neurons or motor circuits. Here we show that song motor nuclei are an exception to this pattern. The song nuclei of species from all known vocal learning avian lineages showed motor-driven up-regulation of dusp1 expression induced by singing. There was no detectable motor-driven dusp1 expression throughout the rest of the forebrain after non-vocal motor performance. This pattern contrasts with expression of the commonly studied activity-induced gene egr1, which shows motor-driven expression in song nuclei induced by singing, but also motor-driven expression in adjacent brain regions after non-vocal motor behaviors. In the vocal non-learning avian species, we found no detectable vocalizing-driven dusp1 expression in the forebrain. These findings suggest that independent evolutions of neural systems for vocal learning were accompanied by selection for specialized motor-driven expression of the dusp1 gene in those circuits. This specialized expression of dusp1 could potentially lead to differential regulation of dusp1-modulated molecular cascades in vocal learning circuits.

Male mice song syntax depends on social contexts and influences female preferences.

In 2005, Holy and Guo advanced the idea that male mice produce ultrasonic vocalizations (USV) with some features similar to courtship songs of songbirds. Since then, studies showed that male mice emit USV songs in different contexts (sexual and other) and possess a multisyllabic repertoire. Debate still exists for and against plasticity in their vocalizations. But the use of a multisyllabic repertoire can increase potential flexibility and information, in how elements are organized and recombined, namely syntax. In many bird species, modulating song syntax has ethological relevance for sexual behavior and mate preferences. In this study we exposed adult male mice to different social contexts and developed a new approach of analyzing their USVs based on songbird syntax analysis. We found that male mice modify their syntax, including specific sequences, length of sequence, repertoire composition, and spectral features, according to stimulus and social context. Males emit longer and simpler syllables and sequences when singing to females, but more complex syllables and sequences in response to fresh female urine. Playback experiments show that the females prefer the complex songs over the simpler ones. We propose the complex songs are to lure females in, whereas the directed simpler sequences are used for direct courtship. These results suggest that although mice have a much more limited ability of song modification, they could still be used as animal models for understanding some vocal communication features that songbirds are used for.

Music, emotion, and autobiographical memory: they're playing your song.

Very long-term memory for popular music was investigated. Older and younger adults listened to 20-sec excerpts of popular songs drawn from across the 20th century. The subjects gave emotionality and preference ratings and tried to name the title, artist, and year of popularity for each excerpt. They also performed a cued memory test for the lyrics. The older adults' emotionality ratings were highest for songs from their youth; they remembered more about these songs, as well. However, the stimuli failed to cue many autobiographical memories of specific events. Further analyses revealed that the older adults were less likely than the younger adults to retrieve multiple attributes of a song together (i.e., title and artist) and that there was a significant positive correlation between emotion and memory, especially for the older adults. These results have implications for research on long-term memory, as well as on the relationship between emotion and memory.

BOULANGER, SATIE, AND DEBUSSY: THEIR SPHERES OF INFLUENCE ON FRENCH MELODIE AND AMERICAN ART SONG

This dissertation project explored the spheres of influence on art song by Nadia Boulanger, Erik Satie, and Claude Debussy within Boulangeries, Les Six, and Les Apaches. After World War I, American composers flocked to Paris to study with Boulanger. Boulanger gave her students the confidence to explore their native talents instead of mimicking foreign models. Works by Aaron Copland, Virgil Thomson, Theodore Chanler, John Duke, and Richard Hundley were included in the first dissertation recital on January 31, 2010: The Legacy of Nadia Boulanger: Her Influence on American Song Composers. Satie established a new modern French musical style, and was a catalyst for the formation of Les Six. Ned Rorem came to Paris, and had a close association with Les Six. Works by Satie, and three members of Les Six, Francis Poulenc, Arthur Honegger, Darius Milhaud; and Rorem were featured in the second recital on September 1, 2010: Satie, Selected Members of Les Six, and Rorem in Paris. Debussy was one of the most significant French composers in the late nineteenth century, predating Boulanger and Satie. Young composers exploring new directions were inspired by Debussy, forming the group Les Apaches. The final recital, April 7, 2011, featured works by Debussy and two members of Les Apaches, Maurice Ravel and Manuel de Falla: Debussy: A Catalyst for Les Apaches, Ravel and Falla. Falla‘s less well-known repertoire was presented. This dissertation showed the influence of these three major figures and that they embraced innovation in their own time, along with their followers. Recordings of these three performances may be obtained from the Michelle Smith Performing Arts Library in Clarice Smith Performing Arts Center at the University of Maryland, College Park.

THE ART SONG OF SOUTH AMERICA: AN EXPLORATION THROUGH PERFORMANCE

The repertoire included in this dissertation was presented over the course of three recitals, The Songs of Argentina, The Songs of Brazil, Chile and Venezuela, and The Songs of Perú and Colombia. Each recital was supplemented by written program notes and English translations of the Spanish, Portuguese and Quechua texts. The selections presented in this study was chosen in an effort to pair the works of internationally renowned composers like Argentine composers Alberto Ginastera and Carlos Guastavino, and Brazilian composer Heitor Villa-Lobos, with those of lesser-known composers, including Venezuelan composer Juan Bautista Plaza, Peruvian composers Edgar Valcárcel, Theodoro Valcárcel, and Rosa Mercedes Ayarza de Morales, and Colombian composer Jaime Léon. Each composer represents a milestone in the development of art song composition in South America. All three recitals were recorded and are available on compact discs in the Digital Repository at the University of Maryland (DRUM). This dissertation was completed in May, 2011.

SELECTED AMERICAN VIOLIN WORKS AND THEIR EUROPEAN CONTEXT

For my dissertation, I did a study and performance of American violin works by Charles Ives, Aaron Copland, Leonard Bernstein, and John Corigliano, along with contemporaneous European works by Paul Hindemith, Bela Bartok, Igor Stravinsky, Sergei Prokofiev, and Francis Poulenc. The selected American violin works display the development of a distinctively American style and cover a significant formative period (1914-1963) of American classical music. I intend that the European works form a backdrop for setting in relief any distinctly American qualities possessed by the American works. This is because they cover a similar time period and have significant stylistic affinities and shared influences. My topic stems from a question, "What defines the American Sound?" I attempted to find the answer by looking at the time when American composers consciously searched for their identities, and declared their music to be distinctly American. I found that those distinctive qualities stemmed from three sources: folk music, jazz and hymns. Ives and Copland can be viewed as American in content for their inclusion of such elements, while Bernstein and Corigliano can also be considered as "ideologically American" for their adventurous and eclectic spirit. The simplicity derived from singing a hymn or crooning a popular song; the freedom inspired by jazz; the optimism of accepting all possibilities-these elements inform the common spirit that I found in the music of these four American composers. FIRST RECITAL Sonatafor Violin Solo Op.3112 (1924), Paul Hindemith (1895-1963) Suite Italiennefor Violin and Piano (1932), Igor Stravinsky (1882-1971) Sonatafor Violin and Piano (1963), John Corigliano (b.1938) SECOND RECITAL Second Sonatafor Violin and Piano (1914-17), Charles Ives (1874-1954) First Rhapsody for Violin and Piano (1928), Bela Bart6k (1881-1971) Violin Sonata No.1 infminor (1938-46), Sergei Prokofiev (1891-1953) THIRD RECITAL Nocturne for Violin and Piano (1926), Aaron Copland (1900-1990)Sonata for Violin and Piano, Op. 119 (1942-3, rev.1949), Francis Poulenc (1899-1963)Serenade (after Plato's "Symposium'') (1954) by Leonard Bernstein (1918-1990) The pianists were Sun Ha Yoon (Bart6k) and Grace Eunae Cho (all other repertoire).

Core and Shell Song Systems Unique to the Parrot Brain.

The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot "core" song system is similar to the song systems of songbirds and hummingbirds, whereas the "shell" song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.

SELECTED TWENTIETH-CENTURY BRITISH & AMERICAN ENGLISH SONG REPERTOIRE WRITTEN FOR SOPRANO

English language song (both British and American) is influenced by a variety of cultures, races, and musical forms and has produced a broad range of song repertoire. Like songs in all countries and throughout history, these songs can be classified into three categories: imitative songs, experimental songs, and songs of individuality. Music experimentation, necessary and welcome as it is, can hardly command broad international attention. Thus, the songs of this dissertation performance project are chosen from the first and third categories: imitative songs and individual songs in the composer's own unique style. This project concentrates its exploration on twentieth-century solo songs written in English. Although twentieth-century British & American composers also produced solos and chamber music in other languages, this dissertation focuses upon their English repertoire. This performance project consists of three programs: one British repertoire and two American. The first program titled An Evening of British Song examines twentieth-century British song written by Roger Quilter, Peter Warlock, William Walton, Benjamin Britten, Thomas F. Dunhill, Ivor Gurney, and Frank Bridge. It was presented on December 12, 2001, in Homer Ulrich Recital Hall with the collaborative pianist Meriel Owen. The second program titled An Evening of American Song I comprises music written by Dominick Argento, Samuel Barber, Ned Rorem, Leonard Bernstein, and Lee Hoiby. It was presented on October 23, 2002, in Joseph & Alma Gildenhorn Recital Hall with the collaborative pianist R. Timothy McReynolds. The third program titled An Evening of American Song II written by John Duke, John Corigliano, Charles Ives, Richard Hundley, Lori Laitman, Frederick Loewe, George Gershwin, and Jerome Kern was presented on December 18, 2003, again in Joseph & Alma Gildenhorn Recital Hall with the collaborative pianist R. Timothy McReynolds and the flutist Jessica Dunnavant. Each of these three dissertation recitals occurred at the University of Maryland in College Park and was recorded. These CD recordings are held by the Michelle Smith Performing Arts Library at the University of Maryland.

LUCIANO BERIO’S NATURALE: A STORY COMBINING FOLK MUSIC AND ART MUSIC

The study of a score by a serious performer is a fundamental step in the process of arriving at a knowledgeable and deeply informed approach to performing a piece of music. In order to obtain this knowledge numerous aspects of the score must be taken into consideration. It is the intent of this dissertation to gather and analyze the information concerning Naturale, a work written by Luciano Berio in 1985 for viola, percussion and recorded voice, based on Sicilian folk songs. All the aspects surrounding Naturale’s existence are taken into consideration in this study. First, it is important to reflect on Berio’s compositional style and traits, the manner in which he relates his works one to another, what he sees in folk music and his own personal desire to intertwine art music and folk music. For Berio Naturale is not an isolated venture into the realm of mixing folk music and his own avant-garde style; it is instead one of many works resulting from his long-standing relationship with folk music. Another essential aspect in this case is the study of Sicilian folk music itself, and the sources used by Berio to find the songs by which he was inspired. The work is examined section by section with figures showing both excerpts of Naturale as well as the original songs with their translations. An analysis containing harmonic, thematic and formal aspects of the score was developed in order to arrive at a better understanding of the structure and pacing of the piece. For this research the author went to Italy to conduct an interview with Maestro Aldo Bennici, the Sicilian violist for whom Naturale was composed. This interview helped in the discovery of two more songs used by Berio that have not to this point been identified in any other document. Bennici’s outstanding testimony portrayed the expressive character of this music and the evocative imagery behind this score. I hope to bring this knowledge to other performers, that they may fully understand and appreciate the unique beauty and power of Berio’s Naturale.