Early experience shapes vocal neural coding and perception in songbirds

Vocal production and perception form our primary means of communication. The role of experience in the neural processing and perception of vocal sounds is an important issue in our pursuit to understand how we acquire and perceive speech and what goes wrong when we can’t understand speech. A significant body of work exists on the role of experience in the development of speech processing and perception in typical and language-impaired children (Chandrasekaran, Hornickel, Skoe, Nicol, & Kraus, 2009; Johnson, Nicol, Zecker, & Kraus, 2008; Kuhl, 2000, 2004, 2010; Kuhl, Tsao, & Liu, 2003; Russo, Nicol, Zecker, Hayes, & Kraus, 2005; Russo et al., 2008; Tsao, Liu, & Kuhl, 2004; Warrier, Johnson, Hayes, Nicol, & Kraus, 2004; Werker & Tees, 1992; Wible, Nicol, & Kraus, 2005). Speech perception research is informed and complemented by research on the neural processing and perception of vocalizations in animals whose experiences can be controlled and brains can be studied at the resolution of single neurons. Animals that learn vocalizations are particularly advantageous because they offer the opportunity to manipulate and measure learning that is specific to vocal communication and to correlate learned behavior with neural mechanisms that are influenced by experience. Though vocal communication is common among animals, vocal learning is rare. Only humans, some cetaceans, and three clades of birds (parrots, hummingbirds and songbirds) are known to learn their vocalizations (Beecher & Brenowitz, 2005). There is some evidence that elephants and bats may be vocal learners as well (Knornschild, Nagy, Metz, Mayer, & von Helversen, 2010; Poole, Tyack, Stoeger-Horwath, & Watwood, 2005). Of these potential animal models, songbirds are by far the most thoroughly studied, and numerous similarities exist between speech and birdsong (Doupe & Kuhl, 1999). Examples include: 1) developmental sensitive periods for vocal learning (Marler, 1997); 2) learning through imitation of adult models (Marler, 1997; Saar, Mitra, Deregnaucourt, & Tchernichovski, 2008); 3) a dependence of vocal behavior on auditory feedback (Konishi, 2004; Woolley, 2004); 4) individual recognition via unique vocalizations (Catchpole & Slater, 2008; Gentner, 2004); and 5) lateralized vocal processing in sensory and sensorimotor brain regions (George, Cousillas, Richard, & Hausberger, 2005; Hauber, Cassey, Woolley, & Theunissen, 2007; Poirier, Boumans, Verhoye, Balthazart, & Van der Linden, 2009; Williams, Crane, Hale, Esposito, & Nottebohm, 1992). Because of the parallels between speech and birdsong and the evolutionary conservation of vocal processing circuitry (Reiner, Perkel, Mello, & Jarvis, 2008; Reiner, Yamamoto, & Karten, 2005; Wang, Brzozowska-Prechtl, & Karten, 2010), the songbird has emerged as a promising model system for studying the neural basis of learned vocal communication. Brain mechanisms of vocal perception are a current research focus due, in part, to increased awareness of neurological disorders that include impaired speech perception, such as autism, Asperger Syndrome and auditory processing disorder. Studies published in the last decade indicate that the vocal communication sounds heard early in life provide experience that is needed for the normal development of the auditory system and, consequently, for perceptual processes that underlie vocal communication. Here, I review studies that address how developmental experience shapes auditory perception and the neural coding of sound in songbirds. The role of experience in songbird vocal production and motor coding have been extensively reviewed elsewhere (Brainard, 2004; Doupe, Perkel, Reiner, & Stern, 2005; Fee & Scharff, 2010; Konishi, 2010; Margoliash, 2010; Mooney, 2009), but I will briefly discuss this topic because it is tightly linked to perceptual development.