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, 30 (5), 934-45

Blood Oxygen Level-Dependent Signal Responses in Corticolimbic 'Emotions' Circuitry of Lactating Rats Facing Intruder Threat to Pups

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Blood Oxygen Level-Dependent Signal Responses in Corticolimbic 'Emotions' Circuitry of Lactating Rats Facing Intruder Threat to Pups

Benjamin C Nephew et al. Eur J Neurosci.

Abstract

Lactating rats must continuously maintain a critical balance between caring for pups and aggressively responding to nest threats. We tested the neural response of lactating females to the presentation of their own pups and novel intruder males using blood oxygen level-dependent functional magnetic resonance imaging at 7 T. Dams were presented with a single sequence of a control stimulus, pups or a male intruder in one imaging session (n = 7-9). To further determine the selectivity of neural processing, dams were imaged for their response to a male intruder in both the absence and presence of their pups (n = 6). Several maternal cortical and limbic brain regions were significantly activated by intruder presentation but not by pups or a control stimulus. These included the nucleus accumbens, periaqueductal gray, anterior cingulate, anterior thalamus, basal nucleus of the amygdala, temporal cortex, prelimbic/orbital area and insula. The nucleus accumbens, periaqueductal gray, temporal cortex and mediodorsal thalamus still showed greater neural activity when compared with intruder presentation in the absence of pups. The present results suggest that the high emotional state generated by a threat to pups involves robust activation of classical limbic regions controlling emotional responses. This pattern of blood oxygen level-dependent activity may precede behavioral states upon which lactating rats initiate attacks against a potential threat to offspring.

Figures

Figure 1
Figure 1
Composite 2D brain maps showing positive BOLD signal changes in response to presentation cradle (no pups), cradle with pups and intruder in the presence of pups. Scale bar hue (orange-to-yellow) indicates percent increase in BOLD with a lower threshold cut-off of 2%. Various regions of interest are highlighted to the left of the figure. Right column highlights BOLD activation in the nucleus accumbens in the pup/intruder condition.
Figure 2
Figure 2
Composite 3D volume brain maps showing positive BOLD signal changes in response to presentation cradle (no pups), cradle with pups and intruder in the presence of pups. Data are shown for the nucleus accumbens and limbic prefrontal cortical areas (upper row) and septal-hippocampal formation regions (lower row). Right column highlights the volume of BOLD activation in the nucleus accumbens in the pup/intruder condition.
Figure 3
Figure 3
Number of positive BOLD voxels in several regions of interested implicated in maternal behavior in rats (Numan, 2007). The three stimulus conditions for each panel are the same as in Figure 1–3. Data are expressed as median (minimum-maximum). Statistical posthoc tests were done with Bonferroni multiple comparisons test. * indicates p < 0.05; † indicates p < 0.01 and + indicates p < 0.001. Left panel black line under graph highlights differences in BOLD activation in the nucleus accumbens. Abbreviations: NAcc, nucleus accumbens; CeA, central amygdala; MeA, medial amygdala; BNST, bed nucleus stria terminalis; PVN, paraventricular nucleus; PAG, periaqueductal grey.
Figure 4
Figure 4
Number of positive BOLD voxels in several regions of interested corresponding to the Papez circuitry (1944). The three stimulus conditions for each panel are the same as in Figure 1–3. Data are expressed as median (minimum-maximum). Statistical posthoc tests were done with Bonferroni multiple comparisons test. * indicates p < 0.05; † indicates p < 0.01 and + indicates p < 0.001. Abbreviations: Acing, anterior cingulate; EntCtx, entorhinal cortex; DG, dentate gyrus; SUB, subiculum; MB, mammillary bodies; AT, anterior thalamus.
Figure 5
Figure 5
Number of positive BOLD voxels in several regions of interested corresponding to the additional limbic circuitry known for their roles in emotional responses (Maclean, 1952). The three stimulus conditions for each panel are the same as in Figure 1–3. Data are expressed as median (minimum-maximum). Statistical posthoc tests were done with Bonferroni multiple comparisons test. * indicates p < 0.05; † indicates p < 0.01 and + indicates p < 0.001. Abbreviations: BAmyg, basonuclei of amygdala; LAmygd, lateral amygdala; LH, lateral hypothalamus; Spt, septum; DS, dorsal striatum; TC, temporal cortex; Prl, prelimbic area; IL, infralimbic area; VO, ventral orbital area; INS, insular cortex.
Figure 6
Figure 6
Composite 2D brain maps showing positive BOLD signal changes in response to presentation of a male intruder in the presence and absence of pups. Scale bar hue (orange-to-yellow) indicates percent increase in BOLD with a lower threshold cut-off of 2%. Various regions of interest are highlighted to the left of the figure.
Figure 7
Figure 7
Number of positive BOLD voxels in several regions of interest compared in Figure 3 to 5. The stimulus conditions for each panel are the same as in Figure 6. Data are expressed as median (minimum- maximum). * indicates p -0.05and + indicates p = 0.01. Abbreviations: NAcc, nucleus accumbens; PAG, periaqueductal grey; BAmyg, basal nucleus of amygdala; Spt, septum; DS, dorsal striatum; TC, temporal cortex; Prl, prelimbic area; VO, ventral orbital area; INS, insular cortex; Acing, anterior cingulate; EntCtx, entorhinal cortex; DG, dentate gyrus; AT, anterior thalamus.
Figure 8
Figure 8
Positive BOLD signal changes over time for the prelimbic medial prefrontal cortex, nucleus accumbens and mediodorsal thalamus. The three stimulus conditions for each panel are the same as in Figure 6.

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