The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches

Abstract

The initial establishment of topographic mapping within developing neural circuits is thought to be shaped by innate mechanisms and is primarily independent of experience. Additional refinement within topographic maps leads to precise matching between presynaptic and postsynaptic neurons and is thought to depend on experiential factors during specific sensitive periods in the animal's development. In male zebra finches, axonal projections of the cortical lateral magnocellular nucleus of the anterior neostriatum (lMAN) are critically important for vocal learning. Overall patterns of topographic organization in the majority of these circuits are adult-like throughout the sensitive period for vocal learning and remain stable despite large-scale functional and morphological changes. However, topographic organization within the projection from the core subregion of lMAN (lMAN core ) to the motor cortical robust nucleus of the archistriatum (RA) is lacking at the onset of song development and emerges during the early stages of vocal learning. To study the effects of song-related experience on patterns of axonal connectivity within different song-control circuits, we disrupted song learning by deafening juvenile zebra finches or exposing them to loud white noise throughout the sensitive period for song learning. Depriving juvenile birds of normal auditory experience delayed the emergence of topographic specificity within the lMAN core 3RA circuit relative to age-matched controls, whereas topographic organization within all other projections to and from lMAN was not affected. The projection from lMAN core to RA therefore provides an unusual example of experience-dependent modification of large-scale patterns of brain circuitry, in the sense that auditory deprivation influences the development of overall topographic organization in this pathway.

Early life exposure to noise alters the representation of auditory localization cues in the auditory space map of the barn owl

“…To name a few: in guinea-pigs, LTEN disrupts the topography of the auditory space map (Withington-Wray et al 1990b); in rats, LTEN delays the emergence of adult-like tonotopic organization (Chang and Merzenich 2003); and in song birds, LTEN delays the crystallization of the normal song (Funabiki and Konishi 2003). Importantly, the effects mentioned above resemble the effects obtained under absolute sensory deprivation, like dark rearing or deafening (Withington-Wray et al 1990a;Iyengar and Bottjer 2002;Carriere et al 2007). In the OT of barn owls, neurons do not respond to binaural uncorrelated sounds (Albeck and Konishi 1995;Takahashi and Keller 1994) and they strongly adapt to continuous noise (Gutfreund and Knudsen 2006;Reches and Gutfreund 2008).…”

Limits on Reacquisition of Song in Adult Zebra Finches Exposed to White Noise

“…This measure differs somewhat from the linearity measure developed by Scharff and Nottebohm (1991) in that it does not count transitions at the ends of songs (Foster and Bottjer, 2001;Iyengar and Bottjer, 2002). This means that a perfect linearity score can be achieved even if a bird's song is occasionally truncated at the beginning and end.…”

Differential expression of glutamate receptors in avian neural pathways for learned vocalization

“…We suggest that differential expression in cerebral vocal nuclei of vocal learners could have been stimulated after a mutational event caused a connection from the arcopallium into the brainstem vocal nucleus DM. Because connectivity of brain pathways outside the vocal system is similar to that within the vocal system (Karten, 1967(Karten, , 1968Margoliash et al, 1994;Mello et al, 1998;Iyengar et al, 1999;Farries, 2001;Iyengar and Bottjer, 2002), once the arcopallium is connected with the brainstem vocal nuclei, this presumably can induce a feedback cascade of specializations in a preexisting cerebral network. This hypothesis requires only a few mutational changes that can be selected upon (selection for specific neural connections), followed by normal interactions of neural activity and gene expression in pre-and postsynaptic neurons.…”