Gastrointestinal projection maps of the vagus nerve are specified permanently in the perinatal period

Powley, Terry L.; Martinson, Fred A.; Phillips, Robert; Jones, Sarahlouise; Baronowsky, Elizabeth A.; Swithers, Susan E.

doi:10.1016/s0165-3806(01)00183-3

Cited by 11 publications

(8 citation statements)

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“…As reference cases, the sham-operated rats exhibited the intact patterns of WGA-HRP-labeled afferents in the stomach that have been described previously (e.g., Wang and Powley, 2000;Phillips et al, 2000;Powley et al, 2001). Briefly, the afferents in the controls projected almost exclusively ipsilaterally.…”

Section: Reinnervation Of the Gi Tract By Vagal Afferentsmentioning

confidence: 79%

“…In the case of the stomach, there is indirect evidence (summarized in Powley et al, 2001) that inhibitory or repulsive factors prevent vagal fibers from sprouting and crossing the midline, i.e., the greater curvature, to innervate the contralateral side of the organ. The present observations on afferents also suggest the possibility that vagal regeneration is limited by inhibitory signals.…”

Section: Potential Mechanisms For Efferent Failure Afferent Successmentioning

confidence: 99%

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Long‐term regeneration of abdominal vagus: Efferents fail while afferents succeed

Phillips

Baronowsky

Powley

2002

J of Comparative Neurology

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Vagal afferents regenerate, by 18 weeks after subdiaphragmatic transection, to reinnervate the gut and to differentiate into the two types of terminals normally found in the smooth muscle wall of the gastrointestinal (GI) tract (Phillips et al. [2000] J Comp Neurol. 421:325-346). Regeneration, however, is neither complete nor entirely accurate by 18 weeks. Moreover, the capacity of the vagal efferents to reinnervate the GI tract under comparable conditions has not been evaluated. Therefore, to determine whether a more extended postaxotomy survival interval would (1). result in more extensive reinnervation of smooth muscle, (2). facilitate correction of the inaccuracies of the regenerated axons and terminals, and (3). yield motor as well as sensory reinnervation of GI targets, Sprague-Dawley rats received either complete subdiaphragmatic vagotomies (n = 18) or sham surgeries (n = 12). Physiological endpoints that might normalize as vagal elements regenerated, including body weight, daily food intake, size of first daily meal, and metabolic efficiency, were monitored. At 45 weeks after the vagotomies, the animals were randomly assigned to afferent (wheat germ agglutinin-horseradish peroxidase) or efferent (cholera toxin subunit B-horseradish peroxidase) mapping conditions, and labeled axons and terminals in the stomach and first 8 cm of the small intestine were inventoried in whole-mounts. Afferent regeneration was more extensive at 45 weeks than previously observed at 18 weeks after surgery; however, the amount of GI innervation was still not comparable to the intact pattern of the sham rats. Furthermore, abnormal patterns of sensory organization occurred throughout the reinnervated field, with small bundles of axons forming complex tangles and some individual axons terminating in ectopic locations. The presence of growth cone profiles suggested that vagal reorganization was ongoing even 45 weeks after surgery. In contrast to this relatively extensive, albeit incomplete, sensory reinnervation of the gut, motor fibers had failed to reinnervate the GI tract. Thus, dramatic differences exist in the regenerative capacities of the sensory and motor arms of the vagus under the same surgical and maintenance conditions. Furthermore, the functional measures of disordered energy regulation did not normalize over the 45 weeks during which afferent but not efferent innervation was restored.

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Section: Reinnervation Of the Gi Tract By Vagal Afferentsmentioning

confidence: 79%

Section: Potential Mechanisms For Efferent Failure Afferent Successmentioning

confidence: 99%

Long‐term regeneration of abdominal vagus: Efferents fail while afferents succeed

Phillips

Baronowsky

Powley

2002

J of Comparative Neurology

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“…Based on both in vivo and in vitro data, ghrelin produced a significant increase in BrdU incorporation, suggesting its potential to promote neuronal development and regeneration. Both the organization and phenotype of DMNV neurones projecting to the gastrointestinal tract undergo extensive specification and reorganization in the perinatal period (Powley et al 2001). The molecular mechanisms that control alteration in vagal innervation are not clear.…”

Section: Discussionmentioning

confidence: 99%

Ghrelin stimulates neurogenesis in the dorsal motor nucleus of the vagus

Zhang¹,

Lin²,

Hu³

et al. 2004

The Journal of Physiology

106

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Ghrelin, a gastric peptide hormone, has been reported to regulate growth hormone secretion and energy homeostasis. Here we show that ghrelin promotes neural proliferation in vivo and in vitro in the rat dorsal motor nucleus of the vagus (DMNV). Ghrelin receptor mRNA and immunoreactivity were detected in tissues from DMNV. Systemic administration of ghrelin (130 nmol kg −1 ) significantly increased 5-bromo-2 -deoxyuridine (BrdU) incorporation in the DMNV in adult rats with cervical vagotomy (BrdU positive cells; from 27 ± 4 to 69 ± 14 n = 5, P < 0.05). In vitro, exposure of cultured DMNV neurones to ghrelin significantly increased the percentage of BrdU incorporation into cells in both dose-dependent (10 −9 -10and time-dependent (6 h to 48 h) manners. Ghrelin significantly increased voltage-activated calcium currents in isolated single DMNV neurones from a mean maximal change of 141 ± 26 pA to 227 ± 37 pA. Upon removal of ghrelin, calcium currents slowly returned to baseline. Blocking L-type calcium channels by diltiazem (10 µM) significantly attenuated ghrelin-mediated increments in BrdU incorporation (n = 5, P < 0.05). Ghrelin acts directly on DMNV neurones to stimulate neurogenesis.

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“…Glutamate stimulates gastric motor activities (Yoon et al, 1996) mediated, in part, through N‐methyl‐D‐aspartate (NMDA) receptors (Travagli et al, 1991; Willis et al, 1996; Sivarao et al, 1999) in the dorsal motor nucleus of the vagus (DMNV), which provides parasympathetic innervation of thoracic and abdominal visceral organs (Izzo et al, 1993; Yoon et al, 1996; Sivarao et al, 1999; Powley et al, 2001). The DMNV receives direct projections from the paraventricular nucleus of the hypothalamus (PVN) (Saper et al, 1976; Swanson and Kuypers, 1980), a higher center integrating neuroendocrine and autonomic mechanisms (Swanson and Sawchenko, 1980).…”

mentioning

confidence: 99%

Ultrastructural localization of serotonin 2A and N‐methyl‐D‐aspartate receptors in somata and dendrites of single neurons within rat dorsal motor nucleus of the vagus

Huang

Pickel

2002

J of Comparative Neurology

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Both glutamate and serotonin are potent modulators of autonomic functions involving the nucleus of the solitary tract (NTS) and the dorsal motor nucleus of the vagus (DMNV) at the level of the area postrema. Moreover, many of the dendrites in this NTS region express both N-methyl-D-aspartate (NMDA) and serotonin (5HT) 2A receptors, and some of these dendrites may arise from the adjacent DMNV. Thus, single neurons in DMNV may also express both receptors. To test this hypothesis, we used electron microscopic immunocytochemistry for dual localization of the essential R1 subunit of the NMDA receptor (NR1) and the 5HT2A receptor in rat intermediate DMNV, a region serving mainly gastrointestinal functions. Gold particles representing NR1 and peroxidase reaction product for 5HT2A receptors were seen in the cytoplasm, as well as on distinct segments of the plasma membrane of many dendrites. Of the NR1-labeled dendrites, 31% (254/814) also contained 5HT2A immunoreactivity; among the 5HT2A-labeled dendrites, 52% (254/485) expressed NR1. The 5HT2A labeling was also present in numerous small unmyelinated axons, axon terminals, and glial processes. These profiles were largely without NR1 immunoreactivity, although NR1 was detected in some of the dendrites postsynaptic to 5HT2A-labeled terminals. Our results suggest that calcium entry through NMDA channels and 5HT2A receptor activation may dramatically affect postsynaptic excitability of single neurons in the DMNV. In addition, the findings also indicate that the 5HT2A receptor is strategically positioned for involvement in modulation of the presynaptic release of neurotransmitters affecting the postsynaptic activity of DMNV neurons responsive to NMDA activation.

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Gastrointestinal projection maps of the vagus nerve are specified permanently in the perinatal period

Cited by 11 publications

References 50 publications

Long‐term regeneration of abdominal vagus: Efferents fail while afferents succeed

Long‐term regeneration of abdominal vagus: Efferents fail while afferents succeed

Ghrelin stimulates neurogenesis in the dorsal motor nucleus of the vagus

Ultrastructural localization of serotonin 2A and N‐methyl‐D‐aspartate receptors in somata and dendrites of single neurons within rat dorsal motor nucleus of the vagus

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