Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Abstract

Individual axon arbors within developing neural circuits are remodeled during restricted sensitive periods, leading to the emergence of precise patterns of connectivity and specialized adaptive behaviors. In male zebra finches, the circuit connecting the medial dorsolateral nucleus of the thalamus (DLM) and its cortical target, the lateral magnocellular nucleus of the anterior neostriatum (lMAN), is crucial for the acquisition of a normal vocal pattern during the sensitive period for song learning. The shell subregion of lMAN as well as the entire terminal field of DLM axons within lMAN undergo a striking increase in overall volume during early stages of vocal learning followed by an equally substantial decrease by adulthood, by which time birds have acquired stable song patterns. Because the total number of DLM neurons remains stable throughout this period, the dramatic changes within the overall DLM3lMAN circuit are presumably attributable to dynamic rearrangements at the level of individual DLM axon arbors over the course of vocal learning.To study such rearrangements directly, we reconstructed individual DLM axon arbors in three dimensions at different stages during vocal learning. Unlike axon arbors in other model systems, in which the number of branches increases during development, DLM arbors are unusual in that they have the greatest number of branches at the onset of vocal learning and undergo large-scale retraction during the sensitive period for song learning. Decreases in the degree of overlap between DLM arbors apparently contribute to the increased overall volume of the DLM3lMAN circuit during vocal learning. These developmental changes in DLM axon arbors occur at the height of the sensitive period for vocal learning, and hence may represent either a morphological correlate of song learning or a necessary prerequisite for acquisition of song. Key words: axons; songbirds; vocal learning; topographic; remodeling; terminalsHighly ordered patterns of connectivity within different neural circuits and the specialized behaviors that they subserve emerge during restricted sensitive periods of development. The initial formation of connections between groups of presynaptic and postsynaptic neurons is characterized by considerable specificity; early patterns of axonal connectivity appear to be genetically predetermined and do not depend on sensory experience (Catalano et al., 1991;Crair et al., 1998;Crowley and Katz, 1999). Adult patterns of connectivity emerge at the culmination of sensitive periods during a later activity-dependent phase when sensory experience is thought to refine these neural circuits at the level of individual axon arbors and synapses (Goodman and

Auditory experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches

“…1] also show large net regression during vocal development, although coarse topography is already established in the DLM VM ¡LMAN shell pathway by 20 days of age (Iyengar and Bottjer 2002a). Thus large-scale regression may contribute to refinement of the coarse topographic map in LMAN shell but is not necessary for its initial establishment.…”

“…In contrast to the LMAN core ¡RA projection, coarse topographic organization is already established by 20 days in the efferent pathway from LMAN shell ¡Ad as well as in the thalamic inputs to core and shell regions of LMAN ( Fig. 1A) (Iyengar and Bottjer 2002a;Iyengar et al 1999). Thus transformation from a highly diffuse pattern of connectivity to a topographically organized map is specific to the projection from LMAN core to vocal motor cortex (RA), and this pathway is known to control the production of juvenile song behavior in zebra finches (Aronov et al 2008).…”

Language‐related Cntnap2 gene is differentially expressed in sexually dimorphic song nuclei essential for vocal learning in songbirds

“…Male LMAN shrinks to half of its original volume by ~50d and female LMAN regression follows with a delay of ~10d (Bottjer et al, 1985; Nixdorf-Bergweiler, 1996). In the male, developmental changes after ~30d have been attributed to processes of cell death (Bottjer et al, 1985; Bottjer and Sengelaub, 1989; Korsia and Bottjer, 1989) and subsequent enlargement of remaining LMAN neurons (Nixdorf-Bergweiler, 1998), as well as refinement of afferent (from DLM; Iyengar et al, 1999; Iyengar and Bottjer, 2002a) and efferent (to RA; Herrmann and Arnold, 1991; Iyengar et al, 1999) connections. The final stage of regression of male LMAN also coincides with the time when lesions of this forebrain nucleus begin to lose their effectiveness in disrupting vocal learning (Bottjer et al, 1984).…”

Photoperiodic differences in a forebrain nucleus involved in vocal plasticity: Enkephalin immunoreactivity reveals volumetric variation in song nucleus lMAN but not NIf in male European starlings (Sturnus vulgaris)

“…The decrease in lMAN volume is paralleled by a substantial decline in the numbers of lMAN neurons (Bottjer and Sengelaub, 1989). Moreover, the total number of DLM neurons remains stable throughout this period and the extensive changes in DLM to lMAN circuit are presumably attributable to the dynamic rearrangements at the level of individual DLM axon arbors over the period of song development (Iyengar and Bottjer, 2002). These findings indeed suggest that the volumetric changes in lMAN during song development in juvenile finches are associated with changes in vocal plasticity.…”

“…In zebra finches, lMAN has been shown to have a core and shell architecture (Johnson and Bottjer, 1992; Johnson et al, 1995). Interestingly, during song development in male zebra finches the volume of lMAN shell undergoes a striking increase in overall volume during early stages of vocal learning followed by an equally substantial decrease by adulthood when birds have acquired stable song patterns (Johnson and Bottjer, 1992; Iyengar and Bottjer, 2002). Moreover, male zebra finches were observed to have increased lMAN cell soma at 50 days compared to female zebra finches (Nixdorf-Bergweiler, 1998).…”