Topographic organization of a forebrain pathway involved with vocal learning in zebra finches

Abstract

A serial pathway from a thalamic nucleus (DLM; the medial portion of the dorsolateral nucleus of the anterior thalamus) to a cortical region (lMAN; the lateral magnocellular nucleus of the anterior neostriatum) to a motor-cortical region (RA; the robust nucleus of the archistriatum) is necessary for vocal production during song learning in juvenile zebra finches but not for the recitation of a song already learned by adults. To obtain new information about the possible function of the DLM-->lMAN-->RA pathway in vocal learning, we used anterograde and retrograde tract-tracing techniques (pressure injections of DiI and DiA) to map the pattern of axonal connections between these brain regions in adult male zebra finches. Results revealed two topographically organized pathways that traverse the songbird forebrain in parallel. An oval-shaped dorsal/lateral portion of DLM projects solely to the central core of lMAN (lMANcore), whereas a crescent-shaped region, including ventral and medial DLM, projects exclusively to a parvicellular shell that encircles lMANcore (lMANshell). In turn, lMANshell neurons project solely to an arc-shaped region of dorsal archistriatum just lateral to RA (Ad; archistriatum, pars dorsalis), whereas lMANcore neurons project exclusively to RA. We also identified crossed and reciprocal pathways between lMANcore/shell and the lateral portion of the ventral archistriatum, which may contribute to interhemispheric coordination of vocal behavior. A robust topographic organization was observed in the axonal projections from dorsal/lateral-DLM-->lMANcore-->RA and from ventral/medial-DLM-->lMANshell-->Ad, raising the question of what is being mapped within these two forebrain pathways. Because RA projection neurons are organized myotopically with respect to the major vocal (syringeal) muscles (D.S. Vicario, 1991, J. Comp. Neurol. 309:486-494), one possibility is that a mapping of vocal/expiratory musculature is preserved "upstream" within these pathways. Similarly, the presence of song-selective auditory neurons in DLM, lMAN, and RA (A.J. Doupe and M. Konishi, 1991, Soc. Neurosci. Abstr. 18:527) suggests that these pathways might subserve some form of auditory or auditory-motor mapping.

Neurotrophins Suppress Apoptosis Induced by Deafferentation of an Avian Motor-Cortical Region

“…5A). This pattern of silver grain labeling over RA is identical to that observed when the lMAN3 RA projection is labeled with anterograde tract-tracing dyes (Bottjer et al, 1989;Johnson et al, 1995). In contrast, birds that received [ 125 I]NT-4/5 showed no specific accumulation of silver grains over RA (C ), indicating that NT-4/5 is not anterogradely transported by lMAN axons.…”

“…The failure of NT-4/5 to be transported is significant, because it indicates specificity in the uptake and /or anterograde transport mechanisms of lMAN neurons. Interestingly, none of the [ 125 I]neurotrophins that we infused were transported in the retrograde direction by the axons of thalamic and cortical brain regions that send projections to lMAN (i.e., from the medial dorsolateral nucleus of the thalamus and from the archistriatum, pars ventralis) (see Johnson et al, 1995). These data demonstrate the selective ability of lMAN axons to anterogradely transport exogenous BDNF and NT-3.…”

“…C, D, High-power images from the central regions of lMANcore and RA show BDNF-immunoreactive somata in lMAN (C) and a fiber in RA (D, arrows), respectively. Because lMAN is the only input to RA that contains BDNF immunoreactive somata, the BDNF-immunoreactive fibers in RA may be the axons of lMANcore neurons (note that the BDNF-immunoreactive fibers appeared to project into RA along the same lateral and dorsolateral orientation followed by most lMANcore axons) (Johnson et al, 1995). E, F, High-power images from the central regions of lMANcore and RA, respectively, show that antibody against NT-3 labeled somata throughout both nuclei.…”

“…The labeled fiber bundles (arrow) were oriented dorsoventrally, and they appeared to pass completely through RA, perhaps projecting to a target ventral to RA. These fiber bundles do not appear to be the axons of lMAN neurons, because lMAN axons enter RA dorsolaterally and laterally (Johnson et al, 1995). B, Immunoreactivity for p75 was found throughout RA and was localized primarily to neuronal somata, although fine labeled processes were sometimes observed.…”

“…Digitized videomicrographs of brain sections from juvenile male zebra finches reacted with antibody against BDNF (A-D) or NT-3 (E, F ); dorsal is up and medial is right. A, A low-power image of lMAN shows that lMAN contains numerous BDNFimmunoreactive somata; lMAN is composed of a magnocellular core surrounded by a parvicellular shell (of which only the core projects to RA) (Johnson et al, 1995) and BDNF-immunoreactive somata were present throughout both regions (the thin line indicates outer borders of lMANcore/shell, and the thicker lines show lamina that define the dorsal and ventral boundaries of the anterior neostriatum). B, Although this low-power image shows that RA did not contain BDNF immunoreactive somata (RA is the distinct oval-shaped region just to the right of center), RA did contain numerous BDNF immunoreactive fibers (D).…”