Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata)

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Abstract
Auditory information is critical for vocal imitation and other elements of social life in songbirds. In zebra finches, neural centers that are necessary for the acquisition and production of learned vocalizations are known, and they all respond to acoustic stimulation. However, the circuits by which conspecific auditory signals are perceived, processed, and stored in long-term memory have not been well documented. In particular, no evidence exists of direct connections between auditory and vocal motor pathways, and two newly identified centers for auditory processing, caudomedial neostriatum (Ncm) and caudomedial hyperstriatum ventrale (cmHV), have no documented place among known auditory circuits. Our goal was to describe anatomically the auditory pathways in adult zebra finch males and, specifically, to show the projections by which Ncm and vocal motor centers may receive auditory input. By using injections of different kinds of neuroanatomical tracers (biotinylated dextran amines, rhodamine-linked dextran amines, biocytin, fluorogold, and rhodamine-linked latex beads), we have shown that, as in other avian groups, the neostriatal field L complex in caudal telencephalon is the primary forebrain relay for pathways originating in the auditory thalamus, i.e., the nucleus ovoidalis complex (Ov). In addition, Ncm and cmHV also receive input from the Ov complex. Ov has been broken down into two parts, the Ov “core” and “shell,” which project in parallel to different targets in the caudal telencephalon. Parts of the field L complex are connected among themselves and to Ncm, cmHV, and caudolateral HV (cIHV) through a complex web of largely reciprocal pathways. In addition, cIHV and parts of the field L complex project strongly to the “shelf” of neostriatum underneath the song control nucleus high vocal center (HVC) and to the “cup” of archistriatum rostrodorsal to another song-control nucleus, the robust nucleus of the archistriatum (RA). We have documented two points at which the vocal motor pathway may pick up auditory signals: the HVC-shelf interface and a projection from cIHV to the nucleus interfacialis (NIf), which projects to HVC. These data represent the most complete survey to date of auditory pathways in the adult male zebra finch brain, and of their projections to motor stations of the song system.