Nucleus taenia (Tn) in birds is a discrete component of a loosely defined archistriatal structure, the posterior and medial archistriatum. By virtue of its hypothalamic projections, the posterior and medial archistriatum is thought to be an avian homolog of the amygdala in mammals. A recent fluorogold (FG) study of avian hippocampus revealed backfilled labels in nucleus Tn, suggesting that this nucleus may indeed be the homolog of mammalian amygdala. In the present study, we sought to characterize nucleus Tn in terms of its connections and function. We used the anterograde tracers Phaseolus vulgaris leucoagglutinin (PHAL) and biotinylated dextran amine (BDA) to map the efferent projections of Tn. The retrograde tracers FG and BDA were used to corroborate the efferent projections and to explore the pattern of afferent inputs to Tn. Finally, we explored the role of Tn in social behavior by observing behavioral changes associated with electrolytic lesions to Tn. The subjects of our studies were ring doves and European starlings, representing two avian orders. When a deposit of anterograde tracer was centered in Tn, it revealed projections to the hypothalamus, following the course of the hypothalamic-occipitomesencephalic tract previously reported in pigeons. The projections were bilateral in ring doves and ipsilateral in starlings. The BDA injections in the archistratum intermedium, lateral to Tn, did not yield the same projectional pattern. Together with corroborative data from FG retrograde experiments, these findings suggest that Tn is probably the primary origin of the hypothalamic projection. A robust projection to the hyperstriatal region was present along the lateral wall of the lateral ventricle, continuing into the anteroventral pole of the ventricle. Highly arborized terminal fields were found all along this pathway, notably in the medial parolfactory lobe (corresponding to the basal ganglia) and along the dorsal roof of the rostral hyperstriatum ventrale just ventral to the laminal frontalis superior (in ring doves) and the lamina frontalis suprema (in starlings). Projections to the hippocampal complex were mostly restricted to the parahippocampus. The FG data suggest the presence of afferent projections from the ovoidais shell and nucleus subrotundus region, the hippocampal complex in both species, and high vocal nucleus in starlings. Behavioral effects of Tn lesions suggest that nucleus taenia is involved in the control of social behavior through its influence on the affective state. Nucleus taenia thus exhibits many of the structural and functional features of the amygdaloid complex in mammals – that is, subcortical sensory inputs, hippocampal complex connections, and a functional role in adaptive patterns of social behavior.

The connectivity of a region surrounding the established thalamic auditory nuclei, n. ovoidalis (Ov) and n. semilunaris parovoidalis (SPO), was explored in the ring dove by using the anterograde tracers, Phaseolus vulgaris leucoagglutinin (PHAL) and biocytin, and the retrograde tracer, fluorogold. The Ov-SPO surround received a projection from a cell group along the interface of the auditory midbrain and the n. intercollicularis, as revealed with PHAL and biocytin, and was composed of neurons exhibiting a common morphology. These features and the presence of overlapping projections from different portions of the Ov-SPO surround suggest that this region comprises a functionally discrete area, which we term the Ov shell. Single unit recording within the shell established the existence of acoustically responsive units. Both PHAL and fluorogold labeling revealed a robust projection from the Ov shell to the caudomedial hypothalamus. Major telencephalic projections of the shell terminated within the ventral paleostriatal complex, "end-zones" of the field L, the caudomedial hyperstriatum ventrale, and regions immediately dorsal and lateral to the auditory neostriatum. Except for a portion of the shell bordering medial ovoidalis, PHAL injections into the shell also labeled fibers within the caudolateral neostriatum and along the lateral neostriatal rim. The connectivity of the Ov shell suggests that this region may integrate auditory pathways with brain regions associated with endocrine mediated behavior. In addition, the shell may constitute a source of converging input to several levels of central auditory pathways.

Avian vocalizations are generally understood to play a pivotal role in reproductive functions. The role of the hypothalamus in gonadotropin release in higher vertebrates including birds is well established. To date, however, a direct linkage between the neuronal processing of vocal input and the contingent luteinizing hormone (LH) response has not been demonstrated. In this study, using female ring doves, we recorded neuronal activity from hypothalamic nuclei that, as we have shown previously, receive acoustic inputs from the auditory thalamic relay. Concurrently with recording single-unit responses to stimulation with species-specific coo vocalizations, we sampled LH levels in blood from the pituitary veins. LH concentration in the plasma was significantly elevated in birds hearing species-typical coos but not in birds exposed to experimentally altered coos or white noise or in birds that received no vocal stimulation. We found two types of neurons in the preoptic and anterior hypothalamus that selectively responded to the female nest coo: excitatory units and inhibitory units. Among the excitatory neurons are units characterized by two bursts separated by a period of slow spiking or complete silence, in a pattern approximately corresponding temporally to the two-note coo. We designate them as female-nest-coo-specific units. Most neurons in the posterior hypothalamus were nonselective in their response. Female nest coo and male nest coo stimulation evoked an equal magnitude of discharge changes from responsive units in the preoptic-anterior hypothalamic area. We found, however, that the LH increment was three times greater for birds hearing female nest coos than for birds hearing male nest coos. These observations suggest that feature-detecting neurons such as the female-nest-coo-specific units are involved in gonadotropin-releasing hormone output. The present findings are consistent with the well established behavioral evidence that female nest coos mediate ovarian growth.

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