Behavioral and neurobiological consequences of social subjugation during puberty in golden hamsters

Abstract

In golden hamsters, offensive aggression is facilitated by vasopressin and inhibited by serotonin. We tested whether these neurotransmitter systems respond to modifications resulting from the stress of threat and attack (i.e., social subjugation) during puberty. Male golden hamsters were weaned at postnatal day 25 (P25), exposed daily to aggressive adults from P28 to P42, and tested for offensive aggression as young adults (P45). The results showed a context-dependent alteration in aggressive behavior. Subjugated animals were more likely to attack younger and weaker intruders than nonsubjugated controls. Conversely, subjugated animals were less likely to attack animals of similar size and age. After testing, the animals were killed, and their brains were collected to determine whether these behavioral changes are underlined by changes in the vasopressin and serotonin systems. Social subjugation resulted in a 50% decrease in vasopressin levels within the anterior hypothalamus, a site involved in the regulation of aggression. Furthermore, whereas the density of vasopressin-immunoreactive fibers within the area was not significantly altered in subjugated animals, the number of serotonin-immunoreactive varicosities within the anterior hypothalamus and lateral septum was 20% higher in subjugated animals than in their controls. These results establish puberty as a developmental period sensitive to environmental stressors. Furthermore, the results show that changes in the vasopressin and serotonin systems can correlate with behavioral alterations, supporting the role of these two neurotransmitters in the regulation of aggression.

Fig. 1.

Photomicrographs showing AVP-IR (A) within anterior hypothalamus (AH) and 5-HT-IR (B) within the ventral part of the lateral septum (LSv) of golden hamsters. LV, Lateral ventricle; mSON, medial division of the supraoptic nucleus; NC, nucleus circularis; SCN, suprachiasmatic nucleus;oc, optic chiasma. Scale bars: A, 200 μm; B, 50 μm.

Fig. 2.

Aggressive behavior performed toward younger and smaller intruders. Experimental animals (Subjugated,n = 17) were exposed daily to aggressive adult males from P28 to P42, whereas control hamsters (n= 17) were placed in empty clean cages. The subjects (Control or Subjugated) were tested for a 10 min period on P45. *p < 0.05, Student’st test; **p < 0.01, Mann–Whitney test.

Fig. 3.

Aggressive behavior performed toward intruders of equal size and age. Experimental animals (Subjugated,n = 12) were exposed daily to aggressive adult males from P28 to P42, whereas control hamsters (n= 12) were placed in empty clean cages. The subjects were tested for a 10 min period on P45. Data from a subset of animals (n = 7 + 7) was used to compare retreats and calculate an aggression index (AI; bites plus attacks minus retreats). *p < 0.05; **p < 0.01, Mann–Whitney tests.

Fig. 4.

Comparison of hypothalamic AVP contents within the anterior hypothalamus of subjugated and control hamsters. Subjugated animals were exposed to aggressive adults during peripubescence. The results are expressed as picograms of AVP per punch taken within the anterior hypothalamus. *p < 0.05, Student’st test.

Fig. 5.

Comparison of the density of 5-HT-IR varicosities within the anterior hypothalamus (AH) and lateral septum (LS) of subjugated (n = 5) versus control (n = 4) hamsters. Varicosities were counted within standard surfaces (15-μm-diameter circles) placed over digitized images. **p < 0.01, Student’st test.