Effects of feeding on in vivo motility patterns in the proximal intestine of shorthorn sculpin (Myoxocephalus scorpius)

Abstract

This is the first study to catalogue the diverse array of in vivo motility patterns in a teleost fish and how they are affected by feeding. Video recordings of exteriorised proximal intestine from fasted and fed shorthorn sculpin (Myoxocephalus scorpius) were used to generate spatio-temporal maps to portray and quantify motility patterns. Propagating and non-propagating contractions were observed to occur at different frequencies and durations. The most apparent difference between the feeding states was that bands of relatively high amplitude contractions propagating slowly in the anal direction were observed in all fasted fish (N=10) but in only 35% of fed fish (N=11). Additionally, fed fish displayed a reduced frequency (0.21±0.03 versus 0.32±0.06 contractions min −1 ) and rhythmicity of these contractions compared with fasted fish. Although the underlying mechanisms of these slow anally propagating contractions differ from those of mammalian migrating motor complexes, we believe that they may play a similar role in shorthorn sculpin during the interdigestive period, to potentially remove food remnants and prevent the establishment of pathogens. 'Ripples' were the most prevalent contraction type in shorthorn sculpin and may be important during mixing and absorption. The persistence of shallow ripples and pendular movements of longitudinal muscle after tetrodotoxin (1 μmol l −1 ) treatment suggests these contractions were myogenic in origin. The present study highlights both similarities and differences in motility patterns between shorthorn sculpin and other vertebrates, as well as providing a platform to examine other aspects of gastrointestinal functions in fish, including the impact of environmental changes.

The presence and role of interstitial cells of Cajal in the proximal intestine of shorthorn sculpin (Myoxocephalus scorpius)

“…Recently, we described a diverse array of in vivo motility patterns in adult shorthorn sculpin (Myoxocephalus scorpius) for the first time (Brijs et al, 2014). Many of the motility patterns were reminiscent of, and/ or may have similar functions to motility patterns documented in other vertebrates (e.g.…”

“…To date, studies examining gastrointestinal motility in fish, including the effects of various neuropeptides and other signalling substances, have primarily used in vitro models (isolated segments of gut; Gräns and Olsson, 2011;Olsson and Holmgren, 2001). Only a few studies have examined the underlying in vivo control mechanisms (Brijs et al, 2014;Holmberg et al, 2007Holmberg et al, , 2006; Rich et al, 2013). Findings from some of these studies have revealed that although blockade of neural activity (using tetrodotoxin, TTX) abolishes some motility patterns, other patterns persist, indicating that they are myogenic in origin (Brijs et al, 2014;Holmberg et al, 2007).…”

“…Only a few studies have examined the underlying in vivo control mechanisms (Brijs et al, 2014;Holmberg et al, 2007Holmberg et al, , 2006; Rich et al, 2013). Findings from some of these studies have revealed that although blockade of neural activity (using tetrodotoxin, TTX) abolishes some motility patterns, other patterns persist, indicating that they are myogenic in origin (Brijs et al, 2014;Holmberg et al, 2007). The myogenically driven component of gastrointestinal motility patterns in fish has repeatedly been suggested to involve ICC (Brijs et al, 2014;Holmberg et al, 2007;Rich et al, 2013Rich et al, , 2007; however, currently our knowledge regarding the presence, distribution and function of these cells in fish is limited.…”

“…The appearance of these cells corresponds well with the onset of propagating contractions observed in zebrafish larvae (Holmberg et al, 2003), supporting the idea that these Ano1-positive cells may be pacemaker ICC. Furthermore, support for the involvement of ICC in the generation of gastrointestinal motility in fish lies in the fact that shallow propagating contractions ('ripples') observed in shorthorn sculpin share many characteristics with myogenic contractions in mammals (Brijs et al, 2014;D'Antona et al, 2001). However, the majority of the evidence is circumstantial and therefore direct manipulation of ICC activity is required to determine the role of ICC in gastrointestinal motility of fish.…”

“…Furthermore, the functional involvement of ICC in intestinal motor behaviour was investigated using a pharmacological antagonist of Ano1 channels and a previously tested in vivo method for qualitatively and quantitatively measuring motility patterns in teleost fish (Brijs et al, 2014).…”