Intracellular recording from myenteric neurons of the guinea‐pig ileum that respond to stretch

Abstract

Isolated longitudinal muscle‐myenteric plexus preparations from guinea‐pig ileum were used to investigate the activity of myenteric neurons when the tissue was stretched in the circumferential direction. Membrane potentials were recorded via flexibly mounted intracellular recording electrodes containing Neurobiotin in 1 M KCl. The preparations were stretched to constant widths (+20 % and +40 % beyond slack width). Multipolar neurons (Dogiel type II morphology) discharged spontaneous action potentials and proximal process potentials during maintained stretching, three of twenty‐one at +20 % stretch and seven of nine at +40 % stretch. At the maximum extent of stretch tried, +40 % beyond slack tissue width, action potentials in Dogiel type II neurons occurred at 10‐33 Hz. Neurons with other morphologies were all uniaxonal. Some displayed spontaneous fast EPSPs or action potentials, three of forty‐one at +20 % stretch and seven of nineteen at +40 % stretch. In seven of eight Dogiel type II neurons, action potentials or proximal process potentials persisted when membrane hyperpolarization was imposed via the recording electrode. Action potential discharge was abolished by hyperpolarization in seven of nine uniaxonal neurons; the exceptions were two orally projecting neurons. Dogiel type II and uniaxonal neurons were classified as rapidly accommodating if they discharged action potentials only at the beginning of a 500 ms intracellular depolarizing pulse and slowly accommodating if they discharged for more than 250 ms. For Dogiel type II neurons, three of thirteen were slowly accommodating at +20 % stretch and two of four at 40 % stretch. For uniaxonal neurons the corresponding data were twelve of twenty‐six and fifteen of nineteen neurons. The slowly accommodating state was associated with increased cell input resistance in uniaxonal neurons. The spontaneous action potential discharge in Dogiel type II and uniaxonal neurons ceased when the muscle was relaxed pharmacologically by nicardipine (3 μM) or isoprenaline (1 μM), although the applied stretch was maintained. At the same time, evoked spike discharge became rapidly accommodating We conclude that many Dogiel type II neurons, and possibly some orally projecting uniaxonal neurons, are intrinsic, stretch‐sensitive, primary afferent neurons that respond to muscle tension with sustained action potential discharge.

Involvement of TRPV2 Activation in Intestinal Movement through Nitric Oxide Production in Mice

“…( Muraki et al, 2003;Shibasaki et al, 2010). Indeed, many IPANs and some uniaxonal neurons are also reported to be mechanosensitive and activated by muscle contractions in guinea pig intestine (Kunze et al, 1998(Kunze et al, , 1999. Mechanosensitive channels in IPANs and some uniaxonal neurons appear to be Gd 2ϩ insensitive and not pure Ca 2ϩ channels (Furness et al, 2004b), properties similar to those of TRPV2 channels.…”

“…Interestingly, many IPANs and some uniaxonal neurons (mainly excitatory and inhibitory motor neurons) appear to be mechanosensitive and activated by muscle contractions in guinea pig intestine (Kunze et al, 1998(Kunze et al, , 1999. Acetylcholine (ACh) and nitric oxide (NO) are dominant excitatory and inhibitory neurotransmitters, respectively (Harrison and McSwiney, 1936;Rand, 1992), and abnormal NO production or release has been implicated in functional gastrointestinal disorders (Takahashi, 2003).…”

Regulation of Guinea pig intestinal peristalsis by endogenous endothelin acting at ETB receptors

“…Third, the pharmacology of the properistaltic action of BQ-788 likewise points to a muscular location of the ET B receptors. The increase in PPT caused by ET B receptormediated muscle relaxation may result from the effect of relaxation to inhibit the discharge of intrinsic sensory neurons subserving peristalsis 41 or from the effect of relaxation to offset the muscle's ability to contract, as can be deduced from the rise of the residual intraluminal pressure in the presence of STX-6c.…”

Role of α2‐adrenoceptors in the sympathetic inhibition of motility reflexes of guinea‐pig ileum

“…(EPSPs) that partially suppress the characteristic afterhyperpolarizing potentials (AHPs) in the intrinsic sensory neurons (Kunze et al 1998). Thus, intrinsic sensory neurons at the recording site may be in a state of tonic excitation prior to activation of the ascending neural pathways.…”

“…Thus, there is a basal level of tension in the circular muscle and an ongoing mechanical stimulus to the mucosa. Rapid reflex responses in the circular muscle to sustained stimuli quickly decline to baseline levels , but the intrinsic sensory neurons continue to fire in response to such stimuli Kunze et al 1998). Furthermore, this firing is accompanied by slow excitatory synaptic potentials Figure 9.…”