Auditory information is important for social and reproductive behaviors in birds generally, but is crucial for oscine species (songbirds), in particular because in these species auditory feedback ensures the learning and accurate maintenance of song. While there is considerable information on the auditory projections through the forebrain of songbirds, there is no information available for projections through the brainstem. At the latter levels the prevalent model of auditory processing in birds derives from an auditory specialist, the barn owl, which uses time and intensity parameters to compute the location of sounds in space, but whether the auditory brainstem of songbirds is similarly functionally organized is unknown. To examine the songbird auditory brainstem we charted the projections of the cochlear nuclei angularis (NA) and magnocellularis (NM) and the third-order nucleus laminaris (NL) in zebra finches using standard tract-tracing techniques. As in other avian species, the projections of NM were found to be confined to NL, and NL and NA provided the ascending projections. Here we report on differential projections of NA and NL to the torus semicircularis, known in birds as nucleus mesencephalicus lateralis, pars dorsalis (MLd), and in mammals as the central nucleus of the inferior colliculus (ICc). Unlike the case in nonsongbirds, the projections of NA and NL to MLd in the zebra finch showed substantial overlap, in agreement with the projections of the cochlear nuclei to the ICc in mammals. This organization could suggest that the “what” of auditory stimuli is as important as “where.”

The avian entopallium (E) is the major thalamorecipient zone, within the telencephalon, of the tectofugal visual system. Because of discrepancies concerning the structure of this nuclear mass in pigeons, and in light of recent evidence concerning entopallial projections in other avian species, we here redefine and chart some novel entopallial projections in the pigeon by using a combination of cytochrome oxidase (CO) activity, calcium binding protein immunohistochemistry (CBPi), normal histology, and tract tracing. We show that 1) E is defined by the accurate overlap of CO activity and the dense terminations of thalamic (rotundal) efferents; 2) the perientopallium (Ep), E's overlying belt region, receives a relatively sparse rotundal input and is a major source of projections to wider regions of the hemisphere; and 3) E can be subdivided into internal (Ei) and external (Ex) portions on the basis of normal histology, CBPi, and differential projections. Thus, Ei, but not Ex, makes a reciprocal connection with a distinct nucleus in the ventrolateral mesopallium and is a major source of projections to the lateral striatum. These findings suggest the necessity for a revision of the original proposal of a strictly serial flow of visual information through the entopallial complex and further regions of the hemisphere and also require a modification of the long-standing view that E is comparable to only one specific lamina (IV) of extrastriate visual cortex of mammals. Rather, E appears to be composed of a variety of neuronal types possibly equivalent to those in several neocortical laminae.

In birds the entopallium (formerly known as the core region of ectostriatum) is the major thalamorecipient zone, within the telencephalon, of the tectofugal visual system. Here we sought to redefine the entopallium in the zebra finch, particularly with respect to a laterally adjacent zone, known as the perientopallium (formerly known as the periectostriatal belt), and to determine its projections. We show that the entopallium can be defined by the almost complete overlap of dense terminations of thalamic rotundal afferents and intense cytochrome oxidase activity and parvalbumin immunoreactivity. The perientopallium, on the other hand, can be defined by relatively sparse projections from nucleus rotundus, a calretinin-positive plexus of nerve fibers, and weak cytochrome oxidase activity and parvalbumin immunoreactivity. Within the entopallium, medial and lateral parts can be distinguished on the basis of cell packing density, differential patterns of parvalbumin immunoreactivity and cytochrome oxidase activity, and different projections. We show that the entopallium projects laterally and diffusely to the perientopallium and nidopallium (formerly the neostriatum) and specifically and densely to a teardrop-shaped nucleus in the ventrolateral mesopallium (formerly known as the hyperstriatum ventrale), here called MVL (abbreviation used as a proper name). This latter projection arises predominantly from medial parts of the entopallium, which also receives a reciprocal projection from MVL, and projects to the lateral striatum. These findings suggest that the entopallium can be divided into medial and lateral parts having different functions, one of which is to provide for an extratelencephalic outflow from the medial part, via the lateral striatum. The findings also challenge the idea that informational flow through the various stations of the telencephalic tectofugal visual system is largely sequential and, together with findings in the chicken (Alpar and Tömböl), suggest instead that further substantial projections to telencephalic visual areas in birds can arise independently from both E (entopallium) and Ep (perientopallial belt).

Sequential to companion articles that report the projections of the cochlear nucleus angularis (NA) and the third-order nucleus laminaris (NL) to the central nucleus of the inferior colliculus (MLd) and to the superior olive (OS) and lateral lemniscal nuclei (LLV, LLI, and LLD) (Krützfeldt et al., J Comp Neurol, this issue), we here describe the projections of the latter group of nuclei using standard tract-tracing methods. OS projects on LLV and both have further ascending projections on LLI, LLD, and MLd. LLV also provides auditory input to the song system, via nucleus uvaeformis, and to the thalamo-telencephalic auditory system, via nucleus ovoidalis (Ov), thus bypassing MLd. The two divisions of LLD (LLDa and LLDp) project across the midline via the commissure of Probst each to innervate the homologous contralateral nucleus and MLd. Both, particularly LLDp, also project on Ov. Injections in LLD and LLV resulted in anterograde labeling of caudal nucleus basorostralis (Bas) in the frontal telencephalon, but retrograde tracing so far suggests that only LLI is a real source of this projection (Wild and Farabaugh [1996] J Comp Neurol 365:306–328). OS and LLV also have descending projections on the ipsilateral NA, NM, and NL, and LLV also projects on OS. The ascending inputs to MLd and more rostral nuclei may contribute importantly to mechanisms of auditory pattern (song) recognition. Consistent with previous studies, some of the descending projections may be inhibitory.

Three nuclei of the lateral lemniscus are present in the zebra finch, ventral (LLV), intermediate (LLI), and dorsal (LLD). LLV is separate from the superior olive (OS): it lies closer to the spinal lemniscus and extends much further rostrally around the pontine periphery. LLI extends from a caudal position ventrolateral to the principal sensory trigeminal nucleus (LLIc) to a rostral position medial to the ventrolateral parabrachial nucleus (LLIr). LLD consists of posterior (LLDp) and anterior (LLDa) parts, which are largely coextensive rostrocaudally, although LLDa lies medial to LLDp. All nuclei are identifiable on the basis of cytochrome oxidase activity. The cochlear nucleus angularis (NA) and the third-order nucleus laminaris (NL) project on OS predominantly ipsilaterally, on LLV and LLI predominantly contralaterally, and on LLD contralaterally only. The NA projections are heavier than those of NL and differ from them primarily in their terminations within LLD: NA projects to LLDp, whereas NL projects to LLDa. In this the projections are similar to those in the barn owl (Takahashi and Konishi [1988] J Comp Neurol 274:212–238), in which time and intensity pathways remain separate as far as the central nucleus of the inferior colliculus (MLd). In contrast, in the zebra finch, although NA and NL projections remain separate within LLD, the projections of LLDa and LLDp become intermixed within MLd (Wild et al., J Comp Neurol, this issue), consistent with the intermixing of the direct NA and NL projections to MLd (Krützfeldt et al., J Comp Neurol, this issue). J. Comp. Neurol. 518:2135–2148, 2010.