Electrical pacemakers of canine proximal colon are functionally innervated by inhibitory motor neurons

1989 ◽  
Vol 256 (3) ◽  
pp. C466-C477 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders
Keyword(s):  
Electrical Activity ◽  
Motor Neurons ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Nerve Fibers ◽  
Pacemaker Activity ◽  
Intracellular Recordings ◽  
Potential Oscillations ◽  
Circular Layer ◽  
Different Populations

Pacemaker activity in the canine proximal colon occurs at the submucosal and myenteric borders of the circular layer [Am. J. Physiol. 252 (Cell Physiol. 21): C215-C224 and C290-C299, 1987]. The present study investigated the neural regulation of rhythmic electrical activity. Spontaneous inhibitory junction potentials (IJPs) were observed in intracellular recordings from circular muscle cells near the myenteric border. The amplitudes of these events decayed with distance through the circular layer. Stimulation at the myenteric plexus surface evoked IJPs that mimicked the spontaneous events. Stimulation at the submucosal surface evoked IJPs in adjacent cells that were of shorter duration and of different waveform than myenteric IJPs. Amplitudes of IJPs evoked by stimulation near either surface decayed with distance from the site of stimulation. The decay functions for IJPs were essentially identical to the decay of spontaneous slow waves or myenteric potential oscillations. Spontaneous and evoked IJPs affected the amplitudes, durations, and patterns of ongoing rhythmic electrical activity. The data suggest that myenteric and submucosal pacemaker populations may be innervated by different populations of inhibitory nerve fibers. Innervation appears to be heterogeneous with dense populations of inhibitory nerve fibers predominantly located in the pacemaker regions. Neural regulations of pacemaker activity influences rhythmic electrical activity throughout the muscularis.

Pacemaker activity in septal structures of canine colonic circular muscle

1990 ◽  
Vol 259 (2) ◽  
pp. G264-G273 ◽  
Author(s):  
S. M. Ward ◽  
K. M. Sanders
Keyword(s):  
Slow Wave ◽  
Electrical Coupling ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Slow Waves ◽  
Pacemaker Activity ◽  
Electrical Measurements ◽  
Morphological Studies ◽  
Circular Layer ◽  
And Function

Morphological and electrophysiological experiments were performed to characterize the pacemaker areas of the circular muscle in the canine proximal colon. Morphological studies showed interstitial cells of Cajal lining the submucosal surface of the circular layer and the septal structures that separate the circular layer into bundles. Electrical measurements suggested that slow waves may propagate into the thickness of the circular muscle in a regenerative manner along the surface of these septa. Removal of the submucosal pacemaker region blocked generation of slow waves in nonseptal regions of the circular muscle, but slow-wave activity continued in the circular muscle near septa. These data suggest that slow-wave pacemaker activity is not limited to a two-dimensional surface at the submucosal surface but extends into the interior of the circular layer along septal invaginations. Experiments were also performed to determine the dominance of pacemaker activity (i.e., septal vs. submucosal), and examples were found in which both areas appeared to initiate slow waves in intact muscles. Other studies showed that slow waves could propagate across septa, suggesting some form of electrical coupling between circular muscle bundles. This study provides a more complete view of the structure and function of pacemaker areas in the canine proximal colon.

Electrical and mechanical interactions between the muscle layers of canine proximal colon

1990 ◽  
Vol 258 (3) ◽  
pp. G484-G491 ◽  
Author(s):  
P. J. Sabourin ◽  
Y. J. Kingma ◽  
K. L. Bowes
Keyword(s):  
Membrane Potential ◽  
Circular Muscle ◽  
Longitudinal Direction ◽  
Proximal Colon ◽  
Slow Waves ◽  
The Other ◽  
Potential Oscillations ◽  
Circular Layer ◽  
Longitudinal Layer ◽  
Membrane Potential Oscillations

Electrical and mechanical interactions between the two smooth muscle layers of canine colon have been studied using a dual sucrose gap apparatus. Muscle samples were dissected into an L-shape, with one leg cut in the circular direction and the other cut in the longitudinal direction. Longitudinal muscle was removed from the circular leg and circular muscle was removed from the longitudinal leg. The bend of the L contained both layers. The activity of the two layers was studied simultaneously under basal conditions, after stimulation by neostigmine and carbachol, and in the presence of tetrodotoxin. Interactions were more common after stimulation and were marked by modification of one layer's mechanical and electrical activity during increased activity in the other layer. Two patterns were commonly observed. First, during a burst of membrane potential oscillations and spike potentials in the longitudinal layer, slow waves in the circular layer developed spike potentials and some slow waves were also prolonged. Second, during a slow-wave cycle in the circular layer, the amplitude of membrane potential oscillations in the longitudinal layer was increased with an associated increase in the incidence of spike potentials. These interactions were associated with contractions of increased strength, which were similar in both layers. All interactions continued after nerve-conduction blockade by tetrodotoxin.

Interstitial cells of Cajal and electrical activity in ganglionic and aganglionic colons of mice

2002 ◽  
Vol 283 (2) ◽  
pp. G445-G456 ◽  
Author(s):  
Sean M. Ward ◽  
Michael D. Gershon ◽  
Kathleen Keef ◽  
Yulia R. Bayguinov ◽  
Cheryl Nelson ◽  
...  
Keyword(s):  
Electrical Activity ◽  
Interstitial Cells Of Cajal ◽  
Circular Muscle ◽  
Interstitial Cells ◽  
Proximal Colon ◽  
Neural Responses ◽  
Wild Type ◽  
Circular Layer ◽  
Excitatory Junction Potentials ◽  
Cells Of Cajal

An antibody directed against Kit protein was used to investigate the distribution of interstitial cells of Cajal (ICC) within the murine colon. The ICC density was greatest in the proximal colon and decreased along its length. The distribution of the different classes of ICC in the aganglionic colons of lethal spotted ( ls/ls) mice was found to be similar in age-matched wild-type controls. There were marked differences in the electrical activities of the colons from ls/ls mutants compared with wild-type controls. In ls/ls aganglionic colons, the circular muscle was electrically quiescent compared with the spontaneous spiking electrical activity of wild-type tissues. In ls/ls aganglionic colons, postjunctional neural responses were greatly affected. Inhibitory junction potentials were absent or excitatory junction potentials inhibited by atropine were observed. In conclusion, the distribution of ICC in the ganglionic and aganglionic regions of the colons from ls/ls mutants appeared similar to that of wild-type controls. The electrical activity and neural responses of the circular layer are significantly different in aganglionic segments of ls/ls mutants.

Colonic Electrical Activity: Concerto for Two Pacemakers

Physiology ◽  
1989 ◽  
Vol 4 (5) ◽  
pp. 176-181
Author(s):  
KM Sanders
Keyword(s):  
Electrical Activity ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Slow Waves ◽  
Potential Oscillations ◽  
Contraction Coupling

In the proximal colon, two discrete pacemaker populations exist: one group of cells generates the 6-cycle/min rhythm known as slow waves;other cells generate a 17-cycle/min rhythm termed myenteric potential oscillations. Summation of these events in the circular muscle provides the signal for escitation-contraction coupling. This article describes the origin and integration of pacemaker activities in the colon.

Patterns of electrical activity and neural responses in canine proximal duodenum

1992 ◽  
Vol 263 (6) ◽  
pp. G887-G894 ◽  
Author(s):  
O. Bayguinov ◽  
F. Vogalis ◽  
B. Morris ◽  
K. M. Sanders
Keyword(s):  
Electrical Activity ◽  
Circular Muscle ◽  
Sphincter Of Oddi ◽  
Electrical Field Stimulation ◽  
Muscle Cells ◽  
Proximal Region ◽  
Inhibitory Neurotransmitter ◽  
Proximal Duodenum ◽  
Circular Layer ◽  
Excitatory Junction Potentials

The patterns of electrical activity and neural inputs to the proximal duodenum between the pyloric sphincter and the sphincter of Oddi were studied in muscles of the dog. Smooth muscle cells in the most proximal region were electrically quiescent, but slow waves were recorded in all regions distal to the first few millimeters. Electrical activity was recorded from circular muscle cells near the myenteric and submucosal surfaces of the circular layer, and slow wave activity was similar in both regions. The nature of neural inputs was also characterized. With electrical field stimulation, responses in cells near the submucosal surface were predominantly excitatory junction potentials (EJPs); near the myenteric border responses were either inhibitory junction potentials (IJPs) or biphasic responses (i.e., small EJPs followed by IJPs). EJPs were blocked by atropine. IJPs were nonadrenergic and noncholinergic (NANC), and several experiments suggested that nitric oxide (NO), or a NO-releasing compound, serves as the inhibitory neurotransmitter in this region. Exogenous NO caused hyperpolarization of membrane potential. IJPs and the hyperpolarization response to NO were sensitive to apamin. These data describe the myogenic mechanisms and neurogenic apparatus that appear to regulate motility in the most proximal region of the duodenum.

Interneuronal and motor patterns during crawling behavior of semi-intact leeches.

1997 ◽  
Vol 200 (9) ◽  
pp. 1369-1381 ◽  
Author(s):  
A P Baader
Keyword(s):  
Motor Neurons ◽  
Behavior Pattern ◽  
Activity Patterns ◽  
Medicinal Leech ◽  
Intracellular Recordings ◽  
Motor Patterns ◽  
Potential Oscillations ◽  
Different Types ◽  
Inhibitory Motor Neurons ◽  
Membrane Potential Oscillations

Semi-intact tethered preparations were used to characterize neuronal activity patterns in midbody ganglia of the medicinal leech during crawling. Extra- and intracellular recordings were obtained from identified interneurons and from motor neurons of the longitudinal and circular muscles during crawling episodes. Coordinated activities of nine excitatory and inhibitory motor neurons of the longitudinal and circular muscles were recorded during the appropriate phases of crawling. Thus, during crawling, the leech uses motor output components known to contribute to other types of behavior, such as swimming or the shortening/local bending reflex. Interneurons with identified functions in these other types of behavior exhibit membrane potential oscillations that are in phase with the behavior pattern. Therefore, the recruitment of neuronal network elements during several types of behavior occurs not only at the motor neuron level but also involves interneurons. This applies even to some interneurons that were previously thought to have dedicated functions (such as cells 204 and 208 and the S cell). The function of neuronal circuitries in producing different types of behavior with a limited number of neurons is discussed.

Stretch-activated neuronal pathways to longitudinal and circular muscle in guinea pig distal colon

2003 ◽  
Vol 284 (2) ◽  
pp. G231-G241 ◽  
Author(s):  
Nick J. Spencer ◽  
Grant W. Hennig ◽  
Terence K. Smith
Keyword(s):  
Guinea Pig ◽  
Motor Neurons ◽  
Circular Muscle ◽  
Distal Colon ◽  
Intracellular Recordings ◽  
Excitatory Junction Potentials ◽  
Descending Interneurons ◽  
Electrical Activities ◽  
Small And Large Intestine

The role of the longitudinal muscle (LM) layer during the peristaltic reflex in the small and large intestine is unclear. In this study, we have made double and quadruple simultaneous intracellular recordings from LM and circular muscle (CM) cells of guinea pig distal colon to correlate the electrical activities in the two different muscle layers during circumferential stretch. Simultaneous recordings from LM and CM cells (<200 μm apart) at the oral region of the colon showed that excitatory junction potentials (EJPs) discharged synchronously in both muscle layers for periods of up to 6 h. Similarly, at the anal region of the colon, inhibitory junction potentials (IJPs) discharged synchronously in the two muscle layers. Quadruple recordings from LM and CM orally at the same time as from the LM and CM anally revealed that IJPs occurred synchronously in the LM and CM anally at the same time as EJPs in LM and CM located 20 mm orally. Oral EJPs and anal IJPs were linearly related in amplitude between the two muscle layers. Spatiotemporal maps generated from simultaneous video imaging of the movements of the colon, combined with intracellular recordings, revealed that some LM contractions orally could be correlated in time with IJPs in CM cells anally. N ω-nitro-l-arginine (l-NA; 100 μM) abolished the IJP in LM, whereas a prominent l-NA-resistant “fast” IJP was always observed in CM. In summary, in stretched preparations, synchronized EJPs in both LM and CM orally are generated by synchronized firing of many ascending interneurons, which simultaneously activate excitatory motor neurons to both muscle layers. Similarly, synchronized IJPs in both LM and CM anally are generated by synchronized firing of many descending interneurons, which simultaneously activate inhibitory motor neurons to both muscle layers. This synchronized motor activity ensures that both muscles around the entire circumference are excited orally at the same time as inhibited anally, thus producing net aboral propulsion.

Changes in electrical and mechanical activity during ontogeny of the canine proximal colon

1996 ◽  
Vol 271 (1) ◽  
pp. G184-G191 ◽  
Author(s):  
S. M. Ward
Keyword(s):  
Membrane Potential ◽  
Circular Muscle ◽  
Electrical Field Stimulation ◽  
Muscle Layer ◽  
Proximal Colon ◽  
Mechanical Activity ◽  
Resting Membrane Potential ◽  
Circular Muscle Layer ◽  
Circular Layer ◽  
Spontaneous Contractions

The ontogenetic development of the circular muscle layer of the canine proximal colon was studied in animals from midway through gestation to 30 days old. With age, there was an increase in resting membrane potential along the submucosal surface and a decrease along the myenteric surface of the circular layer. Coinciding with the changes in membrane potential, slow waves increased in amplitude along the submucosal border and decreased in amplitude along the myenteric border. Muscle strips from animals midway through gestation were mechanically quiescent; however, 1 wk before birth spontaneous activity was observed. Electrical field stimulation of enteric nerves increased spontaneous contractions; this increase in activity was reversed to inhibition by atropine. In the presence of atropine and N omega-nitro-L-arginine or N omega-nitro-L-arginine methyl ester, a noncholinergic excitation was revealed at stimulation frequencies > 5 Hz. The results of these studies provide evidence that the canine proximal colon is spontaneously rhythmic and that a functional innervation to the circular muscle layer exists before birth. The gradient in resting membrane potential across the circular layer is absent at birth but develops within 2-3 wk after parturition.

Effects of membrane potential on electrical slow waves of canine proximal colon

1988 ◽  
Vol 255 (6) ◽  
pp. C828-C834 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders
Keyword(s):  
Membrane Potential ◽  
Circular Muscle ◽  
Input Resistance ◽  
Proximal Colon ◽  
Slow Waves ◽  
Cross Sectional ◽  
Electrical Pulses ◽  
Length Constant ◽  
Circular Layer ◽  
External K

The effects of membrane potential on the waveforms and propagation of slow waves were tested using circular muscles of the canine colon. Studies were conducted with intracellular recording techniques on cross-sectional strips of canine proximal colon. Circular muscle cells near the submucosa generated slow waves that decayed in amplitude as they spread through the circular layer. The membrane potentials of cells were less negative as a function of distance from the submucosal border. Cells near the submucosa were depolarized with elevated external K+ and electrical pulses using the partitioned chamber technique. The waveforms of depolarized submucosal cells were compared with events recorded from cells in the bulk of the circular layer. The waveform changes caused by experimental depolarization were different from the changes in waveform that occur during propagation, suggesting the latter are due to a different mechanism than depolarization. The effects of the membrane potential on syncytial input resistance and length constant were also evaluated. The results of these studies are consistent with the hypothesis that slow-wave propagation across the circular layer in canine proximal colon occurs passively.

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