Central vasopressin V1a receptors modulate neural processing in mothers facing intruder threat to pups

Abstract

Vasopressin V1a receptors in the rat brain have been studied for their role in modulating aggression and anxiety. In the current study blood-oxygen-level-dependent (BOLD) functional MRI was used to test whether V1a receptors modulate neural processing in the maternal brain when dams are exposed to a male intruder. Primiparous females were given an intracerebroventricular (ICV) injection of vehicle or V1a receptor antagonist ([beta-Mercapto-beta,beta-cyclopentamethylenepropionyl(1), O-me-Tyr(2),Arg(8)]-Vasopressin, [corrected] 125 ng/10 microL) 90-120 min before imaging. During fMRI, awake dams were presented with a male intruder threat to pups using a specialized chamber that contained separate compartments for pups and a male intruder. Our results indicate that the number of activated voxels was reduced in the cortical amygdala with V1a receptor blockade, while an increase was observed in the anterior olfactory nucleus and other areas. Dams treated with V1a antagonist showed significantly greater BOLD responses in the anterior olfactory nucleus, infralimbic prefrontal cortex, gustatory cortex, somatosensory cortex, and substantia innominata when presented with a novel male intruder. BOLD responses were reduced in the cortical amygdala and ventromedial hypothalamus. The V1a receptor sensitive areas play roles in the processing of smell, taste and touch and emotional reactivity. Thus one interpretation of the present fMRI data is that vasopressin, acting through V1a receptors, may modulate sensory processing and perhaps coordinate this effect with changes in visceromotor activity during the initial stages of maternal aggressive motivation and/or anxiogenic responses.

Figure 1

Composite coronal brain maps showing positive BOLD signal changes in control and V1a antagonist treated dams presented with a threat to pups. Scale bar hue (red-to-yellow) indicates percent increase in BOLD with a lower threshold cut-off of 1%. Various regions of interest are highlighted to the left of the figure.

Figure 2

Number of positive BOLD voxels in control and V1a antagonist treated dams presented with a threat to pups. Top: Composite 3D brain volume maps showing positive BOLD signal changes in the amygdaloid complex and the olfactory system. Bottom: Number of positive BOLD voxels (mean ± SEM) in the cortical amygdala (COA) and anterior olfactory system (AON) of control and V1a antagonist treated dams. * F = 5.2, p = 0.03 and ** F = 8.6, p = 0.01, single factor analysis of variance.

Figure 3

Positive BOLD signal changes over time for several regions of interest for control and V1a antagonist treated dams presented with a threat to pups. Arrow indicates the point of stimulus presentation during the course of the scans.

Figure 4

Cortical somatosensory and motor activity in dams presented with a threat to pups. Composite 3D brain volume maps showing positive BOLD signal changes in somatosensory cortex and motor cortical areas. Positive BOLD signal changes (mean ± SEM) over time for somatosensory and motor cortical subregions in control and V1a antagonist treated dams presented with a threat to pups. Arrow indicates the point of stimulus presentation during the course of the scans.

Figure 5

Diagram illustrating maternal brain areas that responded to the presentation of an intruder male rat and that were sensitive to V1a receptor blockade. Both positive and negative BOLD signal changes are shown in relation to brain V1a receptor quantities as reported by Ostrowski et al. (1994). Shown below is a color scale indicating V1a receptor levels from none to high. The directions and magnitudes of the observed differences are not indicated.