Lesions of an Avian Forebrain Nucleus That Disrupt Song Development Alter Synaptic Connectivity and Transmission in the Vocal Premotor Pathway

Motor exploration can be an adaptive strategy when behavior fails to achieve an expected outcome. For example, like humans, adult songbirds change their vocal output when auditory feedback is altered or absent. Here, we show that the output of an anterior forebrain pathway (AFP) through the avian basal ganglia directly contributes to the expression of deafening-induced vocal changes in adulthood. Lesioning the output nucleus of this circuit in adult male zebra finches reverses moderate changes in song structure and variability caused by deafening. Furthermore, the results indicate that more severe deafening-induced changes in vocal behavior likely reflect altered function outside the AFP (e.g., within the vocal motor pathway). AFP lesions do not promote recovery if songs are severely deteriorated at the time of lesion even though previous work shows that the AFP is required for such deterioration to emerge. Thus, in birds, as in mammals, the contribution of basal ganglia-thalamic-cortical circuits to motor control may change when feedback is absent or unexpected and includes both "active" and "permissive" roles.

Section: Discussionmentioning

confidence: 99%

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

Nordeen

Nordeen²

2010

“…Lesions of lMAN in juvenile birds induce a significant decrease in the number of synapses made by HVC axon arbors onto RA neurons, indicating that lMAN can modify the HVC3 RA circuit (cf. Herrmann and Arnold, 1991;Kittelberger and Mooney, 1999). The delay in the emergence of topographic organization within the lMAN core 3 RA circuit in DF and WN birds may therefore alter patterning of the HVC3 RA circuit and thereby affect vocal behavior and song learning.…”

Section: Discussionmentioning

confidence: 99%

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

Iyengar

Bottjer

2002

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.

“…Such an error correction role for LMAN also has been invoked to explain the severely disruptive effects of LMAN lesions on song development (cf. Bottjer et al, 1984;Mooney, 1992; but see Kittelberger and Mooney, 1999). Because of its putative role in providing auditory feedback for song learning and adult song maintenance, LMAN has been the site of intensive extracellular electrophysiological analysis of song-evoked auditory responses (Doupe and Konishi, 1991;Doupe, 1997;Solis and Doupe, 1997).…”

Section: Discussionmentioning

confidence: 99%

“…After the recording session, birds were deeply anesthetized with equithesin and transcardially perf used with 0.9% saline for Ͻ5 min, followed by 4% paraformaldehyde (PFA) in 25 mM sodium phosphate buffer for ϳ30 min. Brains were removed and post-fixed in 4% PFA with 30% sucrose overnight, blocked sagittally, and sectioned on a freezing microtome at 60 m. Sections were processed using standard techniques (see K ittelberger and Mooney, 1999). C amera lucida drawings were made using 10ϫ or 63ϫ objectives, and sections were counterstained with cresyl violet to confirm L M ANЈs boundaries.…”

Section: Methodsmentioning

confidence: 99%

Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity

Rosen

Mooney

2000

Self Cite

The development, maintenance, and perception of learned vocalizations in songbirds are likely to require auditory neurons that respond selectively to song. Neurons with song-selective responses have been described in several brain nuclei critical to singing, but the mechanisms by which such response properties arise, are modified, and propagate are poorly understood. The lateral magnocellular nucleus of the anterior neostriatum (LMAN) is the output of an anterior forebrain pathway (AFP) essential for learning and maintenance of song, processes dependent on auditory feedback. Although neurons throughout this pathway respond selectively to auditory presentation of the bird's own song, LMAN is the last stage at which responses to this auditory information could be transformed before being transmitted to vocal motor areas, where such responses may influence vocal production. Indeed, previous extracellular studies have indicated that LMANЈs auditory selectivity is greater than that at earlier stages of the AFP. To determine whether LMAN local circuitry transforms or simply relays song-related auditory information to vocal control neurons, it is essential to distinguish local from extrinsic contributions to LMANЈs auditory selectivity. In vivo intracellular recordings from LMAN projection neurons, coupled with local circuit inactivation, reveal that much of LMANЈs song selectivity is supplied by its extrinsic inputs, but selective blockade of GABA receptors indicates that local inhibition is required for the expression of song selectivity. Therefore, LMAN neurons receive highly song-selective information, but LMANЈs local circuitry can mask these selective inputs, providing a mechanism for context-dependent auditory feedback.