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. 1997 Jun 1;17(11):4331-40.
doi: 10.1523/JNEUROSCI.17-11-04331.1997.

Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters

C F Ferris  1 , R H Melloni Jr, G Koppel, K W Perry, R W Fuller, Y Delville
Affiliations

Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters

C F Ferris et al. J Neurosci. .

Abstract

Studies in several species of rodents show that arginine vasopressin (AVP) acting through a V1A receptor facilitates offensive aggression, i.e., the initiation of attacks and bites, whereas serotonin (5-HT) acting through a 5-HT1B receptor inhibits aggressive responding. One area of the CNS that seems critical for the organization of aggressive behavior is the basolateral hypothalamus, particularly the anterior hypothalamic region. The present studies examine the neuroanatomical and neurochemical interaction between AVP and 5-HT at the level of the anterior hypothalamus (AH) in the control of offensive aggression in Syrian golden hamsters. First, specific V1A and 5-HT1B binding sites in the AH are shown by in vitro receptor autoradiography. The binding for each neurotransmitter colocalizes with a dense field of immunoreactive AVP and 5-HT fibers and putative terminals. Putative 5-HT synapses on AVP neurons in the area of the AH are identified by double-staining immunocytochemistry and laser scanning confocal microscopy. These morphological data predispose a functional interaction between AVP and 5-HT at the level of the AH. When tested for offensive aggression in a resident/intruder paradigm, resident hamsters treated with fluoxetine, a selective 5-HT reuptake inhibitor, have significantly longer latencies to bite and bite fewer times than vehicle-treated controls. Conversely, AVP microinjections into the AH significantly shorten the latency to bite and increase biting attacks. The action of microinjected AVP to increase offensive aggression is blocked by the pretreatment of hamsters with fluoxetine. These data suggest that 5-HT inhibits fighting, in part, by antagonizing the aggression-promoting action of the AVP system.

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Figures

Fig. 1.
Fig. 1.
AVP and 5-HT receptor binding in the AH of golden hamsters. Shown are autoradiograms of specific binding for [125I]-[d(CH2)5Sar7]AVP (A), a selective AVP V1A receptor antagonist, and (−)[125I]iodocyanopindolol (B), a selective 5-HT1B receptor ligand. The binding shown was performed on contiguous 20 μm coronal sections. The area outlined over the AH in autoradiogram A is the same approximate area shown in the top photomicrograph depicting AVP immunoreactivity in Figure 2. oc, Optic chiasm;PVN, paraventricular nucleus; SCN, suprachiasmatic nucleus.
Fig. 2.
Fig. 2.
Light-field photomicrographs of coronal sections through the golden hamster hypothalamus. Shown are arginine vasopressin (AVP) and serotonin (5-HT) immunoreactivity associated with the anterior hypothalamus (AH). The star shown in theAVP photomicrograph depicts the same approximate area shown in the bottom photomicrograph of 5-HT immunoreactivity. Scale bars: top, 200 μm;bottom, 75 μm. NC, Nucleus circularis;mSON, medial supraoptic nucleus; oc, optic chiasm.
Fig. 3.
Fig. 3.
Photomicrographs of arginine vasopressin (AVP) and serotonin (5-HT) revealed by double-labeling immunocytochemistry. Shown are AVP and 5-HT fluorescent immunoreactivity acquired through laser scanning confocal microscopy. The same single optical plane is shown for both neurochemical signals in the top black and white photographs. The combination of both digitized images is shown in color on the top right panel. The AVP is depicted in bright yellow and the 5-HT appears as ared/orange. A volume-rendered data set of serial optical sections through the AVP neuron denoted with the star is shown in the bottom color photograph. The green stippling is 5-HT varicosities and putative synapses clustered around the red-colored AVP neuron (denoted by thestar). Scale bars: top, 50 μm;bottom, 30 μm.
Fig. 4.
Fig. 4.
Shown are the means and medians of several behavioral measures recorded from six experienced fighters with and without fluoxetine treatment. The latency to bite, the number of bites, and contact time were recorded against an intruder over a 5 min test period. Odor-induced flank marks were recorded in a vacated soiled cage of another male conspecific over a 5 min period. Latency to mount was recorded against a receptive female placed into the cage, and motor activity was recorded in a large open arena divided into quadrants.
Fig. 5.
Fig. 5.
Shown are the means and medians of two measures of offensive aggression. The latency to bite and number of bites were recorded in 10 experienced fighters treated with each of the three injection regimens noted (intraperitoneal injection + anterior hypothalamic microinjection). The behavioral measures were recorded against an intruder over a 10 min test period.
Fig. 6.
Fig. 6.
Neurochemical regulation of offensive aggression: a model showing the hypothetical interaction of serotonin (5-HT) with the arginine vasopressin (AVP) system in the AH. 5-HT fibers originating from neurons in the raphe nucleus innervate populations of AVP neurons localized to the medial supraoptic nucleus (mSON) and nucleus circularis (NC). These AVP neurons have been identified as potential sources of AVP innervation to the AH involved in agonistic behavior. These AVP neurons together with 5-HT neurons from the raphe nucleus impinge on neurons in the AH involved in the facilitation of aggression. The identity (?) of these post-synaptic neurons is unknown. 5-HT is inhibitory (−), working through a 5-HT1B receptor, whereas AVP is excitatory (+), working through a V1A receptor.
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