Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches

Abstract

Dopamine (DA) is produced in numerous brain areas and influences a wide variety of social behaviors, but very few data are available to establish the socially-relevant response properties of most DA populations, which comprise eight cell groups numbered A8-A15. Anatomically, these DA populations are evolutionarily conserved, and all have been identified in both birds and mammals. We now report the Fos responses of tyrosine hydroxylase-immunoreactive (TH-ir; putatively dopaminergic) neurons in the A8-A15 cell groups of male zebra finches following exposure to a control condition or one of six different social stimuli: a heterospecific male, conspecific male, fighting in a mate competition paradigm (which includes both male and female stimuli), a courtship interaction without physical contact, a courtship interaction with physical contact but no mounting, and a courtship interaction with mounting. We found that the DA cell groups exhibit distinctive profiles of responsiveness to social stimuli. Fos induction in A8, A9, A10 and midbrain A11 neurons increased significantly in response to a variety of conspecific stimuli, but not heterospecific stimuli. In contrast, Fos induction in the preoptic A14 neurons was observed specifically in response to sexual interactions, and Fos induction in hypothalamic A11 neurons appears to primarily reflect the performance of courtship singing. Infundibular A12 neurons, which may be involved in stress-related processes, showed the highest level of TH+Fos colocalization in control subjects. This colocalization decreased in response to all conspecific stimuli except fighting, and did not decrease following exposure to a heterospecific male.

Fig. 1

Distribution of A8-A15 TH-ir neurons (putatively dopaminergic) in the zebra finch brain. Small dots represent single neurons and large dots represent five neurons. The drawings are adapted from Mello et al. (1998). Panels A-H correspond respectively to planes A2.6, A2.2, A1.6, A0.8, A0.4, A0.2, P0.6 and P0.2 of the canary atlas (Stokes et al., 1974).

Fig. 2

Immunocytochemical labeling of Fos-ir nuclei (red) and/or TH-ir neurons (green). (A) TH+Fos double-labeling of preoptic A14 neurons in a MOUNT subject. (C) Distribution of TH-ir neurons in the caudal diencephalon (A13 and rostral A11 subpopulation) and ventral tegmental area (VTA; A12) of a COURT subject. DAPI counterstain (quenched) is shown psuedocolored purple. The asterisk corresponds to the location of double-labeled neurons shown in panel E. (D) TH- and Fos-ir neurons in the caudal A11 subpopulation (midbrain central gray; CG) and A8 neurons in the rostral locus coeruleus of a COURT subject. The asterisk corresponds to the location of double-labeled neurons shown in panel F. Scale bars = 25 μm in panels A and B; 500 μm in panel C; 100 μm in panel D; and 50 μm in panels E and F.

Fig. 3

Percentage of TH-ir neurons that are Fos-ir+ (means ± SEM) following various sociosexual interactions in male zebra finches in the (A) A8 population of the rostral locus coeruleus, (B) A9 population of the substantia nigra, (C) A10 population of the ventral tegmental area, (D) A11 subpopulation of the central gray, (E-F) A11 subpopulation of the caudal hypothalamus, (G) A12 population of the tuberoinfundibular hypothalamus, and (H) rostral A14 subpopulation of the preoptic area. Different letters above the error bars denote significant group differences (Fisher's PLSD; P < 0.05) following significant one-way ANOVA. ANOVA results for the rostral A11 subpopulation (D) approach significance (ANOVA F_5,22 = 2.531, P < 0.06). Asterisks denote significant pairwise comparisons between subjects that were engaged in sexual behavior (COURT and MOUNT) versus those that were not (CON, BCW, and MALE; *P < 0.05, **P < 0.01, ***P < 0.001, unpaired t-tests). Groups are as follows: control (CON), heterospecific male stimulus (black-cheeked waxbill; BCW), male stimulus (MALE); mate competition (FIGHT), courtship with no mounting (COURT), and courtship with successful mounting (MOUNT). A separate group of subjects were allowed to court a female through a wire barrier, yielding the correlation between directed songs and double-labeling shown in panel F.