Targeted electrophysiological analysis of viscerofugal neurons in the myenteric plexus of guinea-pig colon

Hibberd, Timothy J.; Spencer, Nick J.; Zagorodnyuk, Vladimir; Chen, B N; Brookes, Simon Jonathan

doi:10.1016/j.neuroscience.2014.04.066

Cited by 12 publications

(10 citation statements)

References 42 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Most viscerofugal neuron input to sympathetic neurons is synaptically driven by other enteric neurons ( Crowcroft et al, 1971 ; Miller and Szurszewski, 1997 ) and is therefore important for sympathetic reflex activation. Indeed, direct intracellular recordings from guinea pig colonic viscerofugal neurons show they receive nicotinic inputs from multiple myenteric neural pathways ( Sharkey et al, 1998 ; Hibberd et al, 2014 ), and immunohistochemical analyses suggest myenteric descending interneurons contribute most cholinergic terminals to viscerofugal nerve cell bodies ( Lomax et al, 2000 ). Thus, viscerofugal neurons are situated to receive outputs of enteric neural pathways.…”

Section: Discussionmentioning

confidence: 99%

A Novel Mode of Sympathetic Reflex Activation Mediated by the Enteric Nervous System

Hibberd

Yew

Chen

et al. 2020

eNeuro

View full text Add to dashboard Cite

Enteric viscerofugal neurons provide a pathway by which the enteric nervous system (ENS), otherwise confined to the gut wall, can activate sympathetic neurons in prevertebral ganglia. Firing transmitted through these pathways is currently considered fundamentally mechanosensory. The mouse colon generates a cyclical pattern of neurogenic contractile activity, called the colonic motor complex (CMC). Motor complexes involve a highly coordinated firing pattern in myenteric neurons with a frequency of ;2 Hz. However, it remains unknown how viscerofugal neurons are activated and communicate with the sympathetic nervous system during this naturally-occurring motor pattern. Here, viscerofugal neurons were recorded extracellularly from rectal nerve trunks in isolated tube and flat-sheet preparations of mouse colon held at fixed circumferential length. In freshly dissected preparations, motor complexes were associated with bursts of viscerofugal firing at 2 Hz that aligned with 2-Hz smooth muscle voltage oscillations. This behavior persisted during muscle paralysis with nicardipine. Identical recordings were made after a 4-to 5-d organotypic culture during which extrinsic nerves degenerated, confirming that recordings were from viscerofugal neurons. Single unit analysis revealed the burst firing pattern emerging from assemblies of viscerofugal neurons differed from individual neurons, which typically made partial contributions, highlighting the importance and extent of ENS-mediated synchronization. Finally, sympathetic neuron firing was recorded from the central nerve trunks emerging from the inferior mesenteric ganglion. Increased sympathetic neuron firing accompanied all motor complexes with a 2-Hz burst pattern similar to viscerofugal neurons. These data provide evidence for a novel mechanism of sympathetic reflex activation derived from synchronized firing output generated by the ENS.

show abstract

Section: Discussionmentioning

confidence: 99%

A Novel Mode of Sympathetic Reflex Activation Mediated by the Enteric Nervous System

Hibberd

Yew

Chen

et al. 2020

eNeuro

View full text Add to dashboard Cite

show abstract

“…In the present study we demonstrated that ChAT+/NOS+ viscerofugal neurons are differentiated from ChAT+/NOS– viscerofugal neurons by their neurochemical content, cell body morphology, and in their spatial distributions in both circumferential and longitudinal axes. In addition, some evidence of functional differences between these populations of viscerofugal neurons has been reported (Hibberd et al, ). Whether these populations of viscerofugal neurons serve different physiological roles remain to be shown.…”

Section: Discussionmentioning

confidence: 99%

Neurochemical characterization of extrinsic nerves in myenteric ganglia of the guinea pig distal colon

Chen

Sharrad

Hibberd

et al. 2014

J of Comparative Neurology

View full text Add to dashboard Cite

show abstract

“…Since CGRP is differentially expressed in enteric neurons of mouse large intestine and spinal afferents in DRG (26), we sought to determine the origin of CGRP␣-mCherry-expressing axons in the large intestine. To do this, we cultured whole colon preparations for 5 days using the protocol described by Hibberd et al (16), to determine whether mCherry was expressed in nerve fibers of enteric or of spinal sensory neurons. Whole colon preparations were incised along the longitudinal axis, then pinned to the base of a Sylgard-lined petri dish (Dow Corning, Midland, MI) filled with phosphate-buffered saline (PBS; 0.15 M NaCl, 0.01 M NaH 2PO4, pH 7.2).…”

Section: Generation Of Cgrp␣-mcherry Reporter Micementioning

confidence: 99%

Imaging activation of peptidergic spinal afferent varicosities within visceral organs using novel CGRPα-mCherry reporter mice

Spencer

Sorensen

Travis

et al. 2016

American Journal of Physiology-Gastrointestinal and Liver Physi

View full text Add to dashboard Cite

In vertebrates, visceral pain from internal organs is detected by spinal afferents, whose cell bodies lie in dorsal root ganglia (DRG). Until now, all recordings from spinal afferents have been restricted to recording transmission of action potentials along axons, or from cell bodies lying outside their target organ, which is not where sensory transduction occurs. Our aim was to record directly from a major class of spinal afferent within visceral organs, where transduction of sensory stimuli into action potentials occurs. Using novel calcitonin gene-related peptide (CGRP)α reporter mice, DRG neurons expressed mCherry, including nerve axons within viscera. In colon, a minority of total CGRP immunoreactivity was attributed CGRPα. In isolated unstretched colon, calcium imaging from CGRPα-expressing varicose axons did not detect resolvable calcium transients. However, noxious levels of maintained circumferential stretch to the colon induced repetitive calcium transients simultaneously in multiple neighboring varicosities along single mCherry-expressing axons. Discrete varicosities could generate unitary calcium transients independently of neighboring varicosities. However, axons expressing mCherry only generated coordinated calcium transients when accompanied by simultaneous activation of multiple varicosities along that axon. Simultaneous imaging from different classes of myenteric neurons at the same time as mCherry-expressing axons revealed coordinated calcium transients in multiple myenteric neurons, independent of activity in mCherry-expressing axons. CGRPα-expressing axon terminals preferentially responded to heat, capsaicin, and low pH. We show that direct recordings can be made from the major class of peptidergic spinal afferent that contributes to visceral nociception. This approach can provide powerful insights into transduction of stimuli in viscera.

show abstract

Targeted electrophysiological analysis of viscerofugal neurons in the myenteric plexus of guinea-pig colon

Cited by 12 publications

References 42 publications

A Novel Mode of Sympathetic Reflex Activation Mediated by the Enteric Nervous System

A Novel Mode of Sympathetic Reflex Activation Mediated by the Enteric Nervous System

Neurochemical characterization of extrinsic nerves in myenteric ganglia of the guinea pig distal colon

Imaging activation of peptidergic spinal afferent varicosities within visceral organs using novel CGRPα-mCherry reporter mice

Contact Info

Product

Resources

About