Attention and Motivated Response to Simulated Male Advertisement Call Activates Forebrain Dopaminergic and Social Decision-Making Network Nuclei in Female Midshipman Fish

Abstract

Little is known regarding the coordination of audition with decision-making and subsequent motor responses that initiate social behavior including mate localization during courtship. Using the midshipman fish model, we tested the hypothesis that the time spent by females attending and responding to the advertisement call is correlated with the activation of a specific subset of catecholaminergic (CA) and social decision-making network (SDM) nuclei underlying auditory- driven sexual motivation. In addition, we quantified the relationship of neural activation between CA and SDM nuclei in all responders with the goal of providing a map of functional connectivity of the circuitry underlying a motivated state responsive to acoustic cues during mate localization. In order to make a baseline qualitative comparison of this functional brain map to unmotivated females, we made a similar correlative comparison of brain activation in females who were unresponsive to the advertisement call playback. Our results support an important role for dopaminergic neurons in the periventricular posterior tuberculum and ventral thalamus, putative A11 and A13 tetrapod homologues, respectively, as well as the posterior parvocellular preoptic area and dorsomedial telencephalon, (laterobasal amygdala homologue) in auditory attention and appetitive sexual behavior in fishes. These findings may also offer insights into the function of these highly conserved nuclei in the context of auditory-driven reproductive social behavior across vertebrates.

Fig. 1

Example micrographs showing nuclei found to have a significant relationship between time attending speaker and TH-ir + cFos colocalization (A–F) or cFos expression (G–L) in transverse sections. Graphed representation of data (n = 12) and Pearson’s correlation results are presented for each region (C,F,I,L). Arrows in A–E indicate cFos-ir colocalized to TH-ir nuclei. (A–C) Periventicular posterior tuberculum (TPp): mean % colocalization of cFos in TH-ir cells is 36.28% ± 5.94%. (D–E) Ventromedial and ventrolateral nuclei of the thalamus (VM-VL): mean % colocalization of cFos in TH-ir cells in VM-VL is 2.2% ± 1.6%. (G–I) Posterior parvocellular preoptic nucleus (PPp) mean number of cFos cells per section is 82.21± 19.8. (J–L) Medial zone of the dorsal telencephalon (Dm): number of cFos cells per section in Dm is 85.8 ± 24.8. Arrows in G–K indicate Fos-ir within areas of interest. Scale bar = 100 µm.

Fig. 2

Example micrographs showing nuclei found to have no significant relationship between time attending speaker and TH-ir + cFos colocalization (A,D,E,J) or cFos expression (A–I). Transverse sections are shown from the ventral telencephalon (V) (A-D): (A) dorsal nucleus of V (Vd), (B) supracommissural nucleus of V (Vs), (C) ventral nucleus of area V (Vv), and (D) postcommissural nucleus of area V (Vp). Diencephalon (E–H): (E) anterior parvocellular preoptic nucleus (PPa), (F) magnocellular preoptic nucleus (PM), (G) central posterior nucleus of the thalamus (CP), (H) anterior tuberal nucleus (AT). Brainstem (I–J): (I) periaqueductal gray (PAG), (J) locus coeruleus (LC). Scale bar = 100 µm.

Fig. 3

Top-down schematic diagrams of correlated activity between catecholaminergic nuclei, social decision-making network (SDM) nodes, and auditory circuitry in responding (A) and nonresponding (B) females during playback of the male advertisement call. Positive Pearson coefficients (r-values) are represented as solid lines, and negative correlations are denoted with dotted lines. All correlations had P-values ≤ 0.0495.