VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord

Ida J. Llewellyn-Smith, Carolyn L. Martin, Natalie M. Fenwick, Stephen E. Dicarlo, Heidi L. Lujan, Ann M. Schreihofer

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

Fast excitatory neurotransmission to sympathetic and parasympathetic preganglionic neurons (SPN and PPN) is glutamatergic. To characterize this innervation in spinal autonomic regions, we localized immunoreactivity for vesicular glutamate transporters (VGLUTs) 1 and 2 in intact cords and after upper thoracic complete transections. Preganglionic neurons were retrogradely labeled by intraperitoneal Fluoro-Gold or with cholera toxin B (CTB) from superior cervical, celiac, or major pelvic ganglia or adrenal medulla. Glutamatergic somata were localized with in situ hybridization for VGLUT mRNA. In intact cords, all autonomic areas contained abundant VGLUT2-immunoreactive axons and synapses. CTB-immunoreactive SPN and PPN received many close appositions from VGLUT2-immunoreactive axons. VGLUT2-immunoreactive synapses occurred on Fluoro-Gold-labeled SPN. Somata with VGLUT2 mRNA occurred throughout the spinal gray matter. VGLUT2 immunoreactivity was not noticeably affected caudal to a transection. In contrast, in intact cords, VGLUT1-immunoreactive axons were sparse in the intermediolateral cell column (IML) and lumbosacral parasympathetic nucleus but moderately dense above the central canal. VGLUT1-immunoreactive close appositions were rare on SPN in the IML and the central autonomic area and on PPN. Transection reduced the density of VGLUT1-immunoreactive axons in sympathetic subnuclei but increased their density in the parasympathetic nucleus. Neuronal cell bodies with VGLUT1 mRNA occurred only in Clarke's column. These data indicate that SPN and PPN are densely innervated by VGLUT2-immunoreactive axons, some of which arise from spinal neurons. In contrast, the VGLUT1-immunoreactive innervation of spinal preganglionic neurons is sparse, and some may arise from supraspinal sources. Increased VGLUT1 immunoreactivity after transection may correlate with increased glutamatergic transmission to PPN.

Original languageEnglish
Pages (from-to)741-767
Number of pages27
JournalJournal of Comparative Neurology
Volume503
Issue number6
DOIs
StatePublished - 20 Aug 2007

Fingerprint

Axons
Spinal Cord
Neurons
Cholera Toxin
Carisoprodol
Synapses
Messenger RNA
Vesicular Glutamate Transport Protein 1
Vesicular Glutamate Transport Protein 2
Vesicular Glutamate Transport Proteins
Adrenal Medulla
Synaptic Transmission
Ganglia
Abdomen
In Situ Hybridization
Thorax
methanesulfonate salt 2-hydroxy-4,4'-diamidinostilbene

Keywords

  • Central autonomic control
  • Immunocytochemistry
  • Intermediolateral cell column
  • Neurotransmission
  • Parasympathetic preganglionic neuron
  • Sacral parasympathetic nucleus
  • Sympathetic preganglionic neuron
  • Ultrastructure

Cite this

Llewellyn-Smith, Ida J. ; Martin, Carolyn L. ; Fenwick, Natalie M. ; Dicarlo, Stephen E. ; Lujan, Heidi L. ; Schreihofer, Ann M. / VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord. In: Journal of Comparative Neurology. 2007 ; Vol. 503, No. 6. pp. 741-767.
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VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord. / Llewellyn-Smith, Ida J.; Martin, Carolyn L.; Fenwick, Natalie M.; Dicarlo, Stephen E.; Lujan, Heidi L.; Schreihofer, Ann M.

In: Journal of Comparative Neurology, Vol. 503, No. 6, 20.08.2007, p. 741-767.

Research output: Contribution to journalArticle

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T1 - VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord

AU - Llewellyn-Smith, Ida J.

AU - Martin, Carolyn L.

AU - Fenwick, Natalie M.

AU - Dicarlo, Stephen E.

AU - Lujan, Heidi L.

AU - Schreihofer, Ann M.

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AB - Fast excitatory neurotransmission to sympathetic and parasympathetic preganglionic neurons (SPN and PPN) is glutamatergic. To characterize this innervation in spinal autonomic regions, we localized immunoreactivity for vesicular glutamate transporters (VGLUTs) 1 and 2 in intact cords and after upper thoracic complete transections. Preganglionic neurons were retrogradely labeled by intraperitoneal Fluoro-Gold or with cholera toxin B (CTB) from superior cervical, celiac, or major pelvic ganglia or adrenal medulla. Glutamatergic somata were localized with in situ hybridization for VGLUT mRNA. In intact cords, all autonomic areas contained abundant VGLUT2-immunoreactive axons and synapses. CTB-immunoreactive SPN and PPN received many close appositions from VGLUT2-immunoreactive axons. VGLUT2-immunoreactive synapses occurred on Fluoro-Gold-labeled SPN. Somata with VGLUT2 mRNA occurred throughout the spinal gray matter. VGLUT2 immunoreactivity was not noticeably affected caudal to a transection. In contrast, in intact cords, VGLUT1-immunoreactive axons were sparse in the intermediolateral cell column (IML) and lumbosacral parasympathetic nucleus but moderately dense above the central canal. VGLUT1-immunoreactive close appositions were rare on SPN in the IML and the central autonomic area and on PPN. Transection reduced the density of VGLUT1-immunoreactive axons in sympathetic subnuclei but increased their density in the parasympathetic nucleus. Neuronal cell bodies with VGLUT1 mRNA occurred only in Clarke's column. These data indicate that SPN and PPN are densely innervated by VGLUT2-immunoreactive axons, some of which arise from spinal neurons. In contrast, the VGLUT1-immunoreactive innervation of spinal preganglionic neurons is sparse, and some may arise from supraspinal sources. Increased VGLUT1 immunoreactivity after transection may correlate with increased glutamatergic transmission to PPN.

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KW - Immunocytochemistry

KW - Intermediolateral cell column

KW - Neurotransmission

KW - Parasympathetic preganglionic neuron

KW - Sacral parasympathetic nucleus

KW - Sympathetic preganglionic neuron

KW - Ultrastructure

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