CNS neurons with links to both mood-related cortex and sympathetic nervous system

Krout, Karl E.; Mettenleiter, Thomas C.; Karpitskiy, Vladimir; Nguyen, Xay Van; Loewy, A.

doi:10.1016/j.brainres.2005.04.090

Cited by 36 publications

(17 citation statements)

References 19 publications

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“…However, this study also shows POMC neurons to be synaptically linked to eWAT and liver. Our studies also show dual-labeled neurons in the NTS, a region known to modulate multiple sympathetic responses (33)(34)(35). We found NTS NPY but not POMC neurons innervate both liver and eWAT, and thus, they may be part of the common outflow to liver and eWAT.…”

Section: Discussionsupporting

confidence: 64%

Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically

Stanley

Pinto

Segal

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

165

134

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The autonomic nervous system regulates fuel availability and energy storage in the liver, adipose tissue, and other organs; however, the molecular components of this neural circuit are poorly understood. We sought to identify neural populations that project from the CNS indirectly through multisynaptic pathways to liver and epididymal white fat in mice using pseudorabies virus strains expressing different reporters together with BAC transgenesis and immunohistochemistry. Neurons common to both circuits were identified in subpopulations of the paraventricular nucleus of the hypothalamus (PVH) by double labeling with markers expressed in viruses injected in both sites. The lateral hypothalamus and arcuate nucleus of the hypothalamus and brainstem regions (nucleus of the solitary tract and A5 region) also project to both tissues but are labeled at later times. Connections from these same sites to the PVH were evident after direct injection of virus into the PVH, suggesting that these regions lie upstream of the PVH in a common pathway to liver and adipose tissue (two metabolically active organs). These common populations of brainstem and hypothalamic neurons express neuropeptide Y and proopiomelanocortin in the arcuate nucleus, melanin-concentrating hormone, and orexin in the lateral hypothalamus and in the corticotrophin-releasing hormone and oxytocin in the PVH. The delineation of this circuitry will facilitate a functional analysis of the possible role of these potential commandlike neurons to modulate autonomic outflow and coordinate metabolic responses in liver and adipose tissue.autonomic nervous system | neuronal tracing | pseudorabies virus T he autonomic nervous system plays a prominent role in modulating carbohydrate and lipid metabolism. The original theories of sympathetic activation (1) proposed a body-wide increase in sympathetic outflow. However, later studies suggested differential sympathetic activation on specific organs through distinct autonomic projections, which permits more finely tuned control of metabolism (2, 3).The liver and adipose tissue play important roles in fuel storage and release. These organs respond to altered energy availability with a set of homeostatic responses mediated by humoral factors and autonomic outflow. For example, activation of hepatic sympathetic aminergic and peptidergic innervation increases glucose output and modulates fatty acid transport. Conversely, parasympathetic activity decreases hepatic glucose output and increases carbohydrate storage (4). Likewise, the sympathetic innervation of white adipose tissue induces lipolysis (5) and alters glucose uptake. Thus, in general, parasympathetic activity favors fuel storage, whereas sympathetic activity increases the fuel available for immediate use.Many CNS regions regulate autonomic outflow to hepatic or adipose tissue to influence peripheral energy homeostasis. In particular, the ventromedial hypothalamus (VMH), dorsomedial hypothalamus (DMH), lateral hypothalamus (LH), and nucleus of the solitary tract (NTS) (6)...

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Section: Discussionsupporting

confidence: 64%

Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically

Stanley

Pinto

Segal

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

165

134

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“…Instead corticosterone is thought to limit the stress response to a novel environment by acting on the hippocampus, as ablation of the hippocampus or transection of the fornix enhances stressinduced fever (23), whereas hippocampal stimulation inhibits corticosterone release (7). However, the limbic system does not communicate directly with the paraventricular nucleus but rather relays information through various nuclei, including those within the AV3V region (13,18). This synaptic relay allows limbic information to be integrated with homeostatic information such as fluid balance and thermoregulatory status prior to the activation of any effector mechanisms.…”

Section: Discussionmentioning

confidence: 99%

Lesions of the anteroventral third ventricle region exaggerate neuroendocrine and thermogenic but not behavioral responses to a novel environment

Whyte¹,

Johnson²

2007

American Journal of Physiology-Regulatory, Integrative and Comp

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of the anteroventral third ventricle region exaggerate neuroendocrine and thermogenic but not behavioral responses to a novel environment. Am J Physiol Regul Integr Comp Physiol 292: R137-R142, 2007. First published August 10, 2006; doi:10.1152/ajpregu.00465.2006.-Mild psychological stressors provoke an acute rise in core temperature (T C), stimulate the hypothalmo-pituitary-adrenocortical (HPA) axis, and induce various stress-related behaviors. In the present study, we examined the effect of ablation of the anteroventral third ventricle region (AV3V) on both physiological and behavioral responses to a novel environment. T C was monitored in male Sprague-Dawley rats, with either sham or AV3V lesions, during a 5-h exposure to a novel environment. Trunk blood was collected, in a second group of rats, for the assessment of plasma levels of ACTH and corticosterone. Novelty-induced grooming and rearing behaviors were assessed in a third group of animals. T C was elevated in all animals after 30 min in the novel environment, but the rise was exaggerated in rats with AV3V lesions (ϳ0.5°C). AV3V-lesion rats maintained a higher core temperature for 2 h before it returned to the same level as the control group. Plasma levels of ACTH and corticosterone were also exaggerated in the AV3V lesion group after 30 min in a novel environment. In contrast to the physiological responses, the behavioral measures of grooming and rearing revealed no differences between the groups. The results from the current study suggest that neurons within the AV3V region exert an inhibitory influence on the HPA axis and fever developed in response to stressful psychological stimuli. They also confirm that the physiological and hormonal components of the stress response are independent of certain behavioral measures of stress.Sprague-Dawley rats; grooming; adrenocorticotropic hormone; corticosterone; temperature; psychological stress FEVER CAN BE ELICITED BY EITHER physical or psychological stressors. While both febrile responses are mediated by PGE 2 (15, 21), there is a growing consensus that physical and psychological stressors utilize different prostaglandin E 2 receptor subtypes (EP 1 -EP 4 ) (25, 33) and separate neural circuits (6, 9, 28) to generate the elevation in core temperature (T C ). For example, physical stressors (e.g., infection, hemorrhage) are relayed directly with effector neurons in the hypothalamus, whereas psychological stressors (e.g., novelty, conditioned fear, restraint), which require comparison with previous experience to obtain biological significance, are first routed through limbic structures.The anteroventral third ventricular (AV3V) region, an anatomic area that encompasses the organum vasculosum of the lamina terminalis, the ventral portion of the median preoptic nucleus (MnPO), the anteroventral periventricular nucleus, and the periventricular hypothalamic nucleus (4), is thought to play a pivotal role in the modulation of LPS-induced fever. Fos-like immunoreactivity is elevated in the AV3V region after intravenou...

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“…Such anatomical evidence would provide novel and significant information further defining brain stem neural circuitry whereby layer 5 projection neurons in the 'visceromotor' subregion of vmPFC have the potential to directly modulate central cardiovascular and related functions in the rat (Neafsey et al, 1993;Uylings et al, 2000Uylings et al, , 2003Groenewegen and Uylings, 2000;Van Eden and Buijs, 2000;Heidbreder and Groenewegen 2003;Vertes, 2004;Krout et al, 2005). Part of this investigation has been reported previously in abstract form (Bacon and Gabbott, 1997).…”

mentioning

confidence: 87%

“…5A. Interconnections between these subcortical nuclei, some of which project directly to the NTS and VLM, are considered to play a significant role in mediating the cardiovascular effects elicited by stimulation of IL cortex and adjacent areas of vmPFC (Verberne et al, 1997;Fisk and Wyss, 2000;Owens and Verberne, 2001;Krout et al, 2005).…”

Section: Pathways From Il 'Visceromotor' Cortex To Nts and Vlmmentioning

confidence: 99%

“…(Bi) Drawing of section from ϩ3.2 mm anterior to B. (Bii) Histological section (same level as Bi) showing the umbra of the BDA injection site (dark DAB-labeled region) volved in the central control of cardiovascular, respiratory and other autonomic functions in the rat (Kubo et al, 1990;Yasui et al, 1991;Dampney, 1994;Murphy et al, 1994;Owens and Verberne, 1996, 2000Owens et al, 1999;Krout et al, 2005;Resstel and Corrêa, 2006a,b). The principal aim of this study was to use tract-tracing methods in combination with immunocytochemical and light/electron microscopical techniques to ascertain whether catecholamine-containing neurons in the NTS and rVLM were post-synaptic targets of descending input from IL cortex.…”

mentioning

confidence: 99%

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Catecholaminergic neurons in medullary nuclei are among the post-synaptic targets of descending projections from infralimbic area 25 of the rat medial prefrontal cortex

Gabbott

Warner

Busby³

2007

Neuroscience

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The medial prefrontal cortex (mPFC) is directly involved in the integration of cognitive and autonomic functions underlying flexible goal-directed behavior (Cechetto and Saper, 1990;Neafsey et al., 1993;Loewy, 1991;Owens et al., 1999;Van Eden and Buijs, 2000;Drevets, 2000;Heidbreder and Groenewegen, 2003). In the rat, the mPFC is composed of the anterior cingulate (ACd, Brodmann area 24b), prelimbic (PL, area 32), infralimbic (IL, area 25), and peduncular (P) cortices (Neafsey et al., 1993;Gabbott et al., 2005;Resstel and Corrêa, 2006b).Anatomical and physiological evidence indicates that areas of dorsal (d) mPFC (ACd and dPL cortices) process cognitive information, whereas regions of ventromedial prefrontal cortex (vmPFC) (vPL, IL and P cortices) are also involved in autonomic and visceral functions, especially, cardiovascular and respiratory activities (Hardy and Mack, 1990;Neafsey, 1990;Loewy, 1991;Neafsey et al., 1993;Spyer, 1994;Fisk and Wyss, 2000;Uylings et al., 2003;Heidbreder and Groenewegen, 2003). Descending efferent projections from vmPFC, in particular IL cortex, innervate a wide range of subcortical autonomic centers, including the nucleus tractus solitarius (NTS) and ventrolateral medulla (VLM), brain stem nuclei strategically involved in cardiopulmonary activities (Agarwal and Calarescu, 1992;Van Giersbergen et al., 1992;Dampney, 1994;Owens and Verberne, 1996, 2000Owens et al., 1999). Indeed, stimulation of the vPL and IL cortices is known to influence arterial blood pressure and blood flow through specific vascular beds (Owens and Verberne, 2001). As a result, the vmPFC has been considered to represent a 'visceromotor' territory of the rodent PFC (Terreberry and Neafsey, 1987;Ruit and Neafsey, 1990;Loewy, 1991;Neafsey et al., 1993; Resstel and Corrêa, 2006a,b).Although the pathways from IL cortex to autonomic centers in the brain stem have been described in previous light microscope studies (Sesack et al., 1989;Hurley et al., 1991;Takagishi and Chiba, 1991;Van Eden and Buijs, 2000;Heidbreder and Groenewegen, 2003;Vertes, 2004;Gabbott et al., 2005), the ultrastructural identities and neurochemical content of the post-synaptic target neurons have not been investigated in detail (Zagon et al., 1994;Torrealba and Müller, 1999). Of specific functional significance is that catecholaminergic neurons in the NTS and rostral ventrolateral medulla (rVLM) are strategically in-*Correspondence to: P. L. A. Gabbott, Department of Biological Sciences, The Open University, Milton Keynes, MK7 6AA UK. Tel: ϩ44-1908-659469; fax: ϩ44-1908-654167. E-mail address: p.l.gabbott@open.ac.uk (P. L. A. Gabbott). Abbreviations: ACd, dorsal anterior cingulate cortex (area 24b); B, Bregma; BDA, biotinylated dextran amine; BLA, basolateral nucleus of the amygdala; CEA, central nucleus of the amygdala; DAB, 3,3=-diaminobenzidine; DMH, dorsomedial hypothalamic nucleus; DMX, dorsal motor nucleus of the vagus; IL, infralimbic cortex (area 25

show abstract

CNS neurons with links to both mood-related cortex and sympathetic nervous system

Cited by 36 publications

References 19 publications

Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically

Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically

Lesions of the anteroventral third ventricle region exaggerate neuroendocrine and thermogenic but not behavioral responses to a novel environment

Catecholaminergic neurons in medullary nuclei are among the post-synaptic targets of descending projections from infralimbic area 25 of the rat medial prefrontal cortex

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