The Journal of Neuroscience, November 1, 1999, 19(21):9385-9398
Lesions of an Avian Forebrain Nucleus That Disrupt Song
Development Alter Synaptic Connectivity and Transmission in the Vocal
Premotor Pathway
J. Matthew
Kittelberger and
Richard
Mooney
Department of Neurobiology, Duke University Medical Center, Durham,
North Carolina 27710
The avian forebrain nucleus, the lateral magnocellular nucleus of
the anterior neostriatum (LMAN), is necessary for normal song
development because LMAN lesions made in juvenile birds disrupt song
production but do not disrupt song when made in adults. Although these
age-limited behavioral effects implicate LMAN in song learning, a
potential confound is that LMAN lesions could disrupt normal vocal
motor function independent of any learning role by altering LMAN's
premotor target, the song nucleus, the robust nucleus of the
archistriatum (RA). To date, however, no studies have examined directly
the effects of LMAN lesions on the circuitry of the RA. We report here
that juvenile LMAN lesions rapidly and profoundly affect RA, altering
synaptic connectivity within this nucleus, including descending inputs
from the song nucleus HVc. Specifically, morphological assays of the dendritic spines of RA projection neurons
and axon terminal boutons arising from HVc show a numerical decline in
the density of connections in RA in LMAN-lesioned juveniles compared
with controls. Concurrently, LMAN lesions alter excitatory transmission
within the juvenile RA: after LMAN lesions, the stimulus-response relationship between HVc fibers and RA neurons steepens, and the amplitude of spontaneous monophasic EPSCs increases. Rather than arresting RA in a juvenile state, LMAN lesions transform the structure and function of RA and its connections, such that it is distinct from
that of the normal juvenile. In many ways, RA circuitry in LMAN-lesioned juveniles resembles that of normal adults, suggesting that LMAN lesions induce a premature maturation of the vocal motor pathway, which may lead to a loss of behavioral plasticity and abnormal
song development.
Key words:
RA; LMAN; lesions; zebra finch; vocal plasticity; song
learning; song nuclei; dendritic spines; homeostatic regulation; excitatory synaptic transmission; trophic effects; synaptic
connectivity
Copyright © 1999 Society for Neuroscience 0270-6474/99/19219385-14$05.00/0