Atypical slow waves generated in gastric corpus provide dominant pacemaker activity in guinea pig stomach

Abstract

When intracellular recordings were made from the circular layer of the intact muscular wall of the isolated guinea pig gastric corpus, an ongoing regular high frequency discharge of slow waves was detected even though this region lacked myenteric interstitial cells. When slow waves were recorded from preparations consisting of both the antrum and the corpus, slow waves of identical frequency, but with different shapes, were generated in the two regions. Corporal slow waves could be distinguished from antral slow waves by their time courses and amplitudes. Corporal slow waves, like antral slow waves, were abolished by buffering the internal concentration of calcium ions, [Ca2+]i, to low levels, or by caffeine, 2-aminoethoxydiphenyl borate or the chloride channel blocker DIDS. Corporal preparations demonstrated an ongoing discharge of unitary potentials, as has been found in all other tissues containing interstitial cells. The experiments show that the corpus provides the dominant pacemaker activity which entrains activity in other regions of the stomach and it is suggested that this activity is generated by corporal intramuscular interstitial cells.

Figure 1. Properties of corporal slow waves

The upper trace (A) shows recordings of corporal slow waves, which were superimposed on a peak negative potential of −53 mV. The upstrokes of corporal slow waves had low rates of membrane potential change with dV/dt_max being about 10 mV s⁻¹ (B). Corporal slow waves were generated at regular intervals at a frequency of about 5 waves min⁻¹ (C); time calibration bar applies to all traces. The micrographs show the distribution of interstitial cells. ICC_IM were detected in the longitudinal (Da) and circular layers (Db) but ICC_MY were not detected in the entire wall of the corpus (Dc); calibration bar in Dc applies to all micrographs.

Figure 2. Comparison between corporal and antral slow waves

The upper left pair of traces shows slow waves (Aa) and their dV/dt (Ab) recorded at the corporal end of a corporal–antral preparation. The upper central pair of traces shows a slow wave (Ba) and associated dV/dt (Bb) displayed with expanded time base; the peak negative potential was −49 mV. The upper right micrograph shows a full wall thickness view of interstitial cells present at the corporal end (C). The lower left pair of traces show slow waves (Ea) and their dV/dt (Eb) recorded at the antral end of the same corporal–antral preparation. The lower central pair of traces shows one of these slow waves with initial component (Fa) and associated dV/dt (Fb) on an expanded time base; peak negative potential was −67 mV. The lower right micrograph shows a full wall thickness view of interstitial cells present at the antral end (G); note that ICC_MY were readily detected in the antrum. Slow waves were generated at the same rate (D) in the corpus (filled circles) and antrum (open circles). All observations were from the same preparation. The calibration bar in G applies to both micrographs.

Figure 3. Properties of isolated bundles of corporal circular muscle

Slow waves recorded from an intact sheet of corpus (A) are compared with those recorded from a bundle of circular muscle (B) isolated from the same preparation. Both preparations displayed ongoing discharges of slow waves which occurred with similar frequencies. The discharge of slow waves in the bundle (B) was abolished by applying 50 μm MAPTA-AM for 10 min (C). A power spectral density curve (open circles), calculated from the membrane potential recording obtained after treating with MAPTA-AM, shows the characteristic form (D), similar to those obtained from other tissues containing ICC_IM: the continuous line shows the best theoretical fit obtained when time constant A had a value of 425 ms and B had a value of 75 ms (Edwards et al. 1999). The peak negative potentials in A, B and C were −50, −48 and −48 mV, respectively. The time and voltage calibration bars apply to traces A–C.

Figure 4. Pharmacological properties of slow waves recorded from isolated bundles of the corpus circular layer

Corporal slow waves were abolished by 1 mm caffeine (A and B), by 50 μm 2APB (C and D) or by 100 μm DIDS (E and F). The time and voltage calibration bars apply to all traces.