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Sensory afferents from the gastrointestinal tract

David Grundy, Tim Scratcherd

10.1002/cphy.cp060116

Source: Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Visceral Nerves as Sensory Nerves
1.1 Pathways to the Central Nervous System
2 Classification of Gastrointestinal Receptors
3 Sensory Code
4 Methodology
5 Mucosal Receptors
5.1 Spontaneous Activity
5.2 Mechanosensitivity
5.3 Receptive Fields
5.4 Chemosensitivity
5.5 Thermoreceptors
6 Muscle Receptors
6.1 In‐Series Tension Receptors
7 Serosal and Mesenteric Receptors
7.1 Receptive Fields
7.2 Spontaneous Activity
7.3 Response Characteristics
8 Functional Specificity and Transduction of Stimuli
9 Spontaneous Activity in Gastrointestinal Afferents
10 Rate of Adaptation
11 Modulation of Receptor Activity
12 Functional Significance of Gastrointestinal Receptors
12.1 Mucosal Receptors
12.2 Muscle Receptors
13 Serosal and Mesenteric Receptors
14 Conclusions
Figure 1. Figure 1.

Effect of brushing on a mucosal unit. Lower trace, force applied measured by a force transducer attached to paintbrush. At each downward displacement, paintbrush was stroked across receptive field (1‐mm2 spot). Because of movement of receptive field, size of force applied cannot be compared quantitatively. Response does not extend beyond brushing period.

From Cottrell and Iggo [55
Figure 2. Figure 2.

Response of a mucosal unit to sustained pressure with a glass probe (bar), placed at the edge (upper spike train) and centrally (lower spike trace) in receptive field. Corresponding response collected as histograms, with 1‐s bin width of 2 repetitions of stimulus for each unit shown below. Left histograms, central probe placement; right histograms, peripheral placement.

From Cottrell and Iggo 55
Figure 3. Figure 3.

Response of a gastric chemoreceptor to irrigation of receptive field with 0.1 N hydrochloric acid. Instantaneous response frequency; each action potential generates a dot, which is plotted according to interval from previous action potential, from which instantaneous frequency is calculated. Bottom, time in seconds.

From Davison 59
Figure 4. Figure 4.

Top: response of an intestinal glucoreceptor to glucose solution (10 g/l) injected into small intestinal lumen and maintained for 1 h. A: response immediately after end of injection; B: after 15 min; C: after 30 min; D: after 1 h. Discharge frequency decreases in B‐D, and activity becomes discontinuous. Bottom: effect of glucose on activity of a glucoreceptor.

From Mei 147
Figure 5. Figure 5.

Impulses in afferent vagal fiber from a tension receptor in the antrum. Upper trace, afferent nerve discharge; lower trace, intragastric pressure. As spontaneous waves of contraction pass over receptive field, firing occurs in afferent nerve. Three small transient waves on lower trace were due to respiration.

From Andrews et al. 16
Figure 6. Figure 6.

Response of a single gastric afferent unit to incremental stepwise increase in intragastric volume. Top trace, instantaneous response frequency; middle trace, intragastric pressure; below that is intragastric volume. Dynamic and static components at each increase in volume.

From Clarke 41
Figure 7. Figure 7.

A: impulses in an afferent vagal fiber from tension receptor in upper corpus. Upper trace, action potentials; lower trace, intragastric volume during 50 ml infusion of 0.9% NaCl. B: interval histograms (left) and interval‐interval “scatter” plots (right) of impulse traffic from tension receptor in gastric corpus. Upper records: spontaneous activity, mean frequency 3.98 impulses/s. Lower trace: activity during static phase of gastric distension, with 15 ml of 0.9% NaCl, mean frequency 9.16 impulses/s. Discharge frequency increases with distension and becomes less irregular.

A from Grundy and Scratcherd 96; B from Scratcherd and Grundy 192
Figure 8. Figure 8.

Impulse activity in duodenal tension receptor. Upper trace: longitudinal tension. Lower trace: frequency histogram, 1‐s bin width.

From Cottrell and Iggo 53
Figure 9. Figure 9.

Stimulus‐response relationship of 2 duodenal tension receptors to static phase of compression. Regression lines were calculated by method of least squares.

From Cottrell and Iggo 53
Figure 10. Figure 10.

Top: receptive fields of 6 slowly adapting splanchnic mechanoreceptors associated with ileum, ileocaecal junction, and mesentery. Each symbol represents 1 unit; distribution of symbols shows receptive fields. Values on right, conduction velocity of afferent fibers. Bottom: response of splanchnic afferent unit with 5 points of mechanical sensitivity (A‐E) near ileocolic junction. At each point, mechanical stimuli were applied with a hand‐held glass probe; left, spike shape; right, spike train.

Top from Morrison 157; bottom from Morrison 156
Figure 11. Figure 11.

Mechanosensitive sites of splanchnic afferent units. Units were excited by pressure applied manually with a small glass rod (tip diam 1–2 mm). A: distribution of mechanosensitive sites along arteries, on colon wall, and in mesentery; 20 axons had 1 mechanosensitive spot and 9 axons had 2. B,C: discharge of 2 afferents to pressure on their mechanosensitive sites. B: slowly adapting unit with resting activity. C: fast‐adapting unit without resting activity. V. mes. inf., inferior mesenteric vein; A. mes. inf., inferior mesenteric artery; Aa. iliacae com., common iliac arteries.

From Blumberg et al. 33
Figure 12. Figure 12.

Typical responses (type I‐IV) of 4 splanchnic afferent units (large signals in specimen records) to distension of colon at intraluminal pressure of 100 mmHg for 1 min. Lower record, intraluminal pressure. Histograms on right, peristimulus time histograms of impulse activity (width bin 1‐s) illustrated on left. Size of signal in D decreased during distension because of movement of nerve bundle in relation to recording electrode.

From Blumberg et al. 33
Figure 13. Figure 13.

Impulses in 2 vagal efferent neurons recorded simultaneously from same nerve strand in response to gastric distension; 4‐min continuous recording. Upper trace, efferent nerve discharge; lower trace, intragastric pressure. One efferent neuron was spontaneously active and was inhibited during gastric distension with 40 ml 0.9% NaCl. Second efferent neuron with action potentials of slightly lower amplitude than first was recruited on distension and discharged phasically in rhythm with fluctuations in intragastric pressure due to antral contractions.

From Scratcherd and Grundy 192
Figure 14. Figure 14.

Response of single splanchnic afferent to colonic distension (black bars, intraluminal pressure 50 mmHg) before (A) and during (B) ischemia of colon. Intervals between distension 12–22 min before ischemia and 8–15 min during ischemia. Bin width of peristimulus time histogram 1 s.

From Haupt et al. 109


Figure 1.

Effect of brushing on a mucosal unit. Lower trace, force applied measured by a force transducer attached to paintbrush. At each downward displacement, paintbrush was stroked across receptive field (1‐mm2 spot). Because of movement of receptive field, size of force applied cannot be compared quantitatively. Response does not extend beyond brushing period.

From Cottrell and Iggo [55


Figure 2.

Response of a mucosal unit to sustained pressure with a glass probe (bar), placed at the edge (upper spike train) and centrally (lower spike trace) in receptive field. Corresponding response collected as histograms, with 1‐s bin width of 2 repetitions of stimulus for each unit shown below. Left histograms, central probe placement; right histograms, peripheral placement.

From Cottrell and Iggo 55


Figure 3.

Response of a gastric chemoreceptor to irrigation of receptive field with 0.1 N hydrochloric acid. Instantaneous response frequency; each action potential generates a dot, which is plotted according to interval from previous action potential, from which instantaneous frequency is calculated. Bottom, time in seconds.

From Davison 59


Figure 4.

Top: response of an intestinal glucoreceptor to glucose solution (10 g/l) injected into small intestinal lumen and maintained for 1 h. A: response immediately after end of injection; B: after 15 min; C: after 30 min; D: after 1 h. Discharge frequency decreases in B‐D, and activity becomes discontinuous. Bottom: effect of glucose on activity of a glucoreceptor.

From Mei 147


Figure 5.

Impulses in afferent vagal fiber from a tension receptor in the antrum. Upper trace, afferent nerve discharge; lower trace, intragastric pressure. As spontaneous waves of contraction pass over receptive field, firing occurs in afferent nerve. Three small transient waves on lower trace were due to respiration.

From Andrews et al. 16


Figure 6.

Response of a single gastric afferent unit to incremental stepwise increase in intragastric volume. Top trace, instantaneous response frequency; middle trace, intragastric pressure; below that is intragastric volume. Dynamic and static components at each increase in volume.

From Clarke 41


Figure 7.

A: impulses in an afferent vagal fiber from tension receptor in upper corpus. Upper trace, action potentials; lower trace, intragastric volume during 50 ml infusion of 0.9% NaCl. B: interval histograms (left) and interval‐interval “scatter” plots (right) of impulse traffic from tension receptor in gastric corpus. Upper records: spontaneous activity, mean frequency 3.98 impulses/s. Lower trace: activity during static phase of gastric distension, with 15 ml of 0.9% NaCl, mean frequency 9.16 impulses/s. Discharge frequency increases with distension and becomes less irregular.

A from Grundy and Scratcherd 96; B from Scratcherd and Grundy 192


Figure 8.

Impulse activity in duodenal tension receptor. Upper trace: longitudinal tension. Lower trace: frequency histogram, 1‐s bin width.

From Cottrell and Iggo 53


Figure 9.

Stimulus‐response relationship of 2 duodenal tension receptors to static phase of compression. Regression lines were calculated by method of least squares.

From Cottrell and Iggo 53


Figure 10.

Top: receptive fields of 6 slowly adapting splanchnic mechanoreceptors associated with ileum, ileocaecal junction, and mesentery. Each symbol represents 1 unit; distribution of symbols shows receptive fields. Values on right, conduction velocity of afferent fibers. Bottom: response of splanchnic afferent unit with 5 points of mechanical sensitivity (A‐E) near ileocolic junction. At each point, mechanical stimuli were applied with a hand‐held glass probe; left, spike shape; right, spike train.

Top from Morrison 157; bottom from Morrison 156


Figure 11.

Mechanosensitive sites of splanchnic afferent units. Units were excited by pressure applied manually with a small glass rod (tip diam 1–2 mm). A: distribution of mechanosensitive sites along arteries, on colon wall, and in mesentery; 20 axons had 1 mechanosensitive spot and 9 axons had 2. B,C: discharge of 2 afferents to pressure on their mechanosensitive sites. B: slowly adapting unit with resting activity. C: fast‐adapting unit without resting activity. V. mes. inf., inferior mesenteric vein; A. mes. inf., inferior mesenteric artery; Aa. iliacae com., common iliac arteries.

From Blumberg et al. 33


Figure 12.

Typical responses (type I‐IV) of 4 splanchnic afferent units (large signals in specimen records) to distension of colon at intraluminal pressure of 100 mmHg for 1 min. Lower record, intraluminal pressure. Histograms on right, peristimulus time histograms of impulse activity (width bin 1‐s) illustrated on left. Size of signal in D decreased during distension because of movement of nerve bundle in relation to recording electrode.

From Blumberg et al. 33


Figure 13.

Impulses in 2 vagal efferent neurons recorded simultaneously from same nerve strand in response to gastric distension; 4‐min continuous recording. Upper trace, efferent nerve discharge; lower trace, intragastric pressure. One efferent neuron was spontaneously active and was inhibited during gastric distension with 40 ml 0.9% NaCl. Second efferent neuron with action potentials of slightly lower amplitude than first was recruited on distension and discharged phasically in rhythm with fluctuations in intragastric pressure due to antral contractions.

From Scratcherd and Grundy 192


Figure 14.

Response of single splanchnic afferent to colonic distension (black bars, intraluminal pressure 50 mmHg) before (A) and during (B) ischemia of colon. Intervals between distension 12–22 min before ischemia and 8–15 min during ischemia. Bin width of peristimulus time histogram 1 s.

From Haupt et al. 109
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Article Title: Sensory afferents from the gastrointestinal tract
 

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David Grundy, Tim Scratcherd. Sensory afferents from the gastrointestinal tract. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 593-620. First published in print 1989. doi: 10.1002/cphy.cp060116