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Distinct BOLD Activation Profiles Following Central and Peripheral Oxytocin Administration in Awake Rats.

Ferris CF, Yee JR, Kenkel WM, Dumais KM, Moore K, Veenema AH, Kulkarni P, Perkybile AM, Carter CS - Front Behav Neurosci (2015)

Bottom Line: These data were compared to OT (1 μg/5 μl) given directly to the brain via the lateral cerebroventricle.The change in BOLD signal to peripheral OT did not show any discernible dose-response.The results from this imaging study do not support a direct central action of peripheral OT on the brain.

View Article: PubMed Central - PubMed

Affiliation: Center for Translational NeuroImaging, Northeastern University , Boston, MA , USA.

ABSTRACT
A growing body of literature has suggested that intranasal oxytocin (OT) or other systemic routes of administration can alter prosocial behavior, presumably by directly activating OT sensitive neural circuits in the brain. Yet there is no clear evidence that OT given peripherally can cross the blood-brain barrier at levels sufficient to engage the OT receptor. To address this issue we examined changes in blood oxygen level-dependent (BOLD) signal intensity in response to peripheral OT injections (0.1, 0.5, or 2.5 mg/kg) during functional magnetic resonance imaging (fMRI) in awake rats imaged at 7.0 T. These data were compared to OT (1 μg/5 μl) given directly to the brain via the lateral cerebroventricle. Using a 3D annotated MRI atlas of the rat brain segmented into 171 brain areas and computational analysis, we reconstructed the distributed integrated neural circuits identified with BOLD fMRI following central and peripheral OT. Both routes of administration caused significant changes in BOLD signal within the first 10 min of administration. As expected, central OT activated a majority of brain areas known to express a high density of OT receptors, e.g., lateral septum, subiculum, shell of the accumbens, bed nucleus of the stria terminalis. This profile of activation was not matched by peripheral OT. The change in BOLD signal to peripheral OT did not show any discernible dose-response. Interestingly, peripheral OT affected all subdivisions of the olfactory bulb, in addition to the cerebellum and several brainstem areas relevant to the autonomic nervous system, including the solitary tract nucleus. The results from this imaging study do not support a direct central action of peripheral OT on the brain. Instead, the patterns of brain activity suggest that peripheral OT may interact at the level of the olfactory bulb and through sensory afferents from the autonomic nervous system to influence brain activity.

No MeSH data available.


The 3D color model at the top depicts the location of the brains that comprise the primary olfactory system in the rat. These areas have been coalesced into a single volume (yellow) as shown in the lower 3D images for intraperitoneal OT (n = 12) and vehicle (n = 12). Areas in red (positive BOLD) and blue (negative BOLD) are the localization of the significantly changed voxels comprising the composite average from the rats in each experimental group.
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Figure 4: The 3D color model at the top depicts the location of the brains that comprise the primary olfactory system in the rat. These areas have been coalesced into a single volume (yellow) as shown in the lower 3D images for intraperitoneal OT (n = 12) and vehicle (n = 12). Areas in red (positive BOLD) and blue (negative BOLD) are the localization of the significantly changed voxels comprising the composite average from the rats in each experimental group.

Mentions: By 20 min post IP OT administration, the number of activated brain areas is considerably reduced as compared to the first 10 min as shown in Table S3 in Supplementary Material. Several of the areas that remain significantly activated are part of the primary olfactory system (POS), e.g., external plexiform layer, glomerular layer, cortical amygdala, and rostral piriform cortex. Figure 4 shows 3D BOLD activation maps for vehicle and OT in the POS. The images at the top are color-coded and labeled for each 3D volume. As in Figure 2, these different volumes are coalesced into a single volume (yellow) showing the location in red of the average of the significant increase in volumes of activation (number of voxels in a ROI) for positive BOLD from all rats for each condition. These data are from the 2.5 mg/kg dose of OT acquired in the first 10 min post injection (see Tables S3 and S4 in Supplementary Material). Note the high activation of both positive and negative BOLD in the olfactory bulb (granular cell layer, glomerular layer, external plexiform layer) with OT treatment as compared to vehicle.


Distinct BOLD Activation Profiles Following Central and Peripheral Oxytocin Administration in Awake Rats.

Ferris CF, Yee JR, Kenkel WM, Dumais KM, Moore K, Veenema AH, Kulkarni P, Perkybile AM, Carter CS - Front Behav Neurosci (2015)

The 3D color model at the top depicts the location of the brains that comprise the primary olfactory system in the rat. These areas have been coalesced into a single volume (yellow) as shown in the lower 3D images for intraperitoneal OT (n = 12) and vehicle (n = 12). Areas in red (positive BOLD) and blue (negative BOLD) are the localization of the significantly changed voxels comprising the composite average from the rats in each experimental group.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585275&req=5

Figure 4: The 3D color model at the top depicts the location of the brains that comprise the primary olfactory system in the rat. These areas have been coalesced into a single volume (yellow) as shown in the lower 3D images for intraperitoneal OT (n = 12) and vehicle (n = 12). Areas in red (positive BOLD) and blue (negative BOLD) are the localization of the significantly changed voxels comprising the composite average from the rats in each experimental group.
Mentions: By 20 min post IP OT administration, the number of activated brain areas is considerably reduced as compared to the first 10 min as shown in Table S3 in Supplementary Material. Several of the areas that remain significantly activated are part of the primary olfactory system (POS), e.g., external plexiform layer, glomerular layer, cortical amygdala, and rostral piriform cortex. Figure 4 shows 3D BOLD activation maps for vehicle and OT in the POS. The images at the top are color-coded and labeled for each 3D volume. As in Figure 2, these different volumes are coalesced into a single volume (yellow) showing the location in red of the average of the significant increase in volumes of activation (number of voxels in a ROI) for positive BOLD from all rats for each condition. These data are from the 2.5 mg/kg dose of OT acquired in the first 10 min post injection (see Tables S3 and S4 in Supplementary Material). Note the high activation of both positive and negative BOLD in the olfactory bulb (granular cell layer, glomerular layer, external plexiform layer) with OT treatment as compared to vehicle.

Bottom Line: These data were compared to OT (1 μg/5 μl) given directly to the brain via the lateral cerebroventricle.The change in BOLD signal to peripheral OT did not show any discernible dose-response.The results from this imaging study do not support a direct central action of peripheral OT on the brain.

View Article: PubMed Central - PubMed

Affiliation: Center for Translational NeuroImaging, Northeastern University , Boston, MA , USA.

ABSTRACT
A growing body of literature has suggested that intranasal oxytocin (OT) or other systemic routes of administration can alter prosocial behavior, presumably by directly activating OT sensitive neural circuits in the brain. Yet there is no clear evidence that OT given peripherally can cross the blood-brain barrier at levels sufficient to engage the OT receptor. To address this issue we examined changes in blood oxygen level-dependent (BOLD) signal intensity in response to peripheral OT injections (0.1, 0.5, or 2.5 mg/kg) during functional magnetic resonance imaging (fMRI) in awake rats imaged at 7.0 T. These data were compared to OT (1 μg/5 μl) given directly to the brain via the lateral cerebroventricle. Using a 3D annotated MRI atlas of the rat brain segmented into 171 brain areas and computational analysis, we reconstructed the distributed integrated neural circuits identified with BOLD fMRI following central and peripheral OT. Both routes of administration caused significant changes in BOLD signal within the first 10 min of administration. As expected, central OT activated a majority of brain areas known to express a high density of OT receptors, e.g., lateral septum, subiculum, shell of the accumbens, bed nucleus of the stria terminalis. This profile of activation was not matched by peripheral OT. The change in BOLD signal to peripheral OT did not show any discernible dose-response. Interestingly, peripheral OT affected all subdivisions of the olfactory bulb, in addition to the cerebellum and several brainstem areas relevant to the autonomic nervous system, including the solitary tract nucleus. The results from this imaging study do not support a direct central action of peripheral OT on the brain. Instead, the patterns of brain activity suggest that peripheral OT may interact at the level of the olfactory bulb and through sensory afferents from the autonomic nervous system to influence brain activity.

No MeSH data available.