Nucleus Taenia of the Amygdala of Birds: Anatomical and Functional Studies in Ring Doves <i>(Streptopelia risoria)</i> and European Starlings <i>(Sturnus vulgaris)</i>

Abstract

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.

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

“…In birds, recent tracing studies demonstrate reciprocal connectivity throughout the same suite of steroid-sensitive areas (identically named, with the exception of the avian medial amygdala, which is known as the nucleus taeniae) Briganti et al, 1996;Balthazart and Absil, 1997;Cheng et al, 1999;Montagnese et al, 2004;Riters and Alger, 2004), and a variety of functional data are now available regarding their roles in overt aggression, agonistic communication, appetitive and consummatory sexual behavior, parental behavior, and nonsexual affiliation Thompson et al, 1998;Goodson et al, 1999Goodson et al, , 2005Riters and Ball, 1999;Absil et al, 2002;Goodson and Evans, 2004;Ruscio and Adkins-Regan, 2004;Charlier et al, 2005). These functional studies have established extensive similarities with other taxa.…”

“…All forebrain components of the social behavior network project to the midbrain central gray, as do preoptic aromatase neurons (Cheng et al, 1999;Absil et al, 2001;Montagnese et al, 2004;Riters and Alger, 2004). The central gray in turn provides direct input to the telencephalic song system (i.e., monosynaptic projections are observed for HVC and RA) (Appeltants et al, 2000).…”

Revised nomenclature for avian telencephalon and some related brainstem nuclei

“…Of note, amygdaloid features of the nucleus taeniae have been shown by recent neurochemical, connectional, developmental. and functional studies (Balthazart et al, 1992(Balthazart et al, , 1998Cheng et al, 1999;Foidart et al, 1999;Lanuza et al, 2000;Cobos et al, 2001b, Absil et al, 2002Roberts et al, 2002). For this reason, the Forum recommended that the nucleus taeniae be renamed the nucleus taeniae of the amygdala (Table 5, Fig.…”

The vertebrate social behavior network: Evolutionary themes and variations

“…2B-C) The social behavior network in birds A wide variety of data have been collected on the neuroendocrine systems of birds, and the avian literature is growing rapidly (Goodson et al, submitted-b). On the whole, the social behavior network in birds exhibits extensive similarities with the mammalian network in its connections, histochemistry, and locations of sex steroid receptors (e.g., Watson and AdkinsRegan, 1989;Balthazart et al, 1994;Balthazart et al, 1996;Briganti et al, 1996;Aste et al, 1998;Cheng et al, 1999;Atoji and Wild, 2004;Goodson et al, 2004a;Montagnese et al, 2004). The pattern of IEG induction that is observed in birds following agonistic interactions is also comparable to that observed in mammals, as are IEG responses to appetitive and consummatory sexual interactions (Kollack-Walker and Newman, 1995;Coolen et al, 1996Coolen et al, , 1997Kollack-Walker et al, 1997;Meddle et al, 1997Meddle et al, , 1999Delville et al, 2000;Tlemcani et al, 2000;Maney and Ball, 2003;Davis and Marler, 2004;Goodson and Evans, 2004;Riters et al, 2004; Goodson et al, submitted-a),.…”

“…These include a vocally-active tegmental field that lies lateral to the PAG and medial to the auditory torus/ inferior colliculus (Phillips et al, 1972;Kennedy, 1975;Jürgens, 1994;Goodson and Bass, 2002) in all classes except Amphibia, in which a comparable vocal site is located at isthmal levels (Wetzel et al, 1985). Other selected references : Northcutt, 1981;Bruce and Neary, 1995;Balthazart et al, 1996;Panzica et al, 1996;Wong, 1997;Coolen and Wood, 1998;Lanuza and Halpern, 1998;Nieuwenhuys et al, 1998;Cheng et al, 1999;Goodson and Bass, 2000c;Dong et al, 2001;Petrovich et al, 2001;Goodson et al, 2003;Moreno and Gonzalez, 2003;Dong and Swanson, 2004;Goodson et al, 2004a;Rink and Wullimann, 2004;…”