Ingestible pills reveal gastric correlates of emotions

  1. Giuseppina Porciello  Is a corresponding author
  2. Alessandro Monti
  3. Maria Serena Panasiti
  4. Salvatore Maria Aglioti  Is a corresponding author
  1. Department of Psychology, Sapienza Università di Roma, Italy
  2. IRCCS Fondazione Santa Lucia Research Hospital, Italy
  3. Sapienza Università di Roma and Center for Life Nano- & Neuro-Science, Fondazione Istituto Italiano di Tecnologia, Italy
14 figures, 11 tables and 1 additional file

Figures

Illustration of the emotional induction procedure.

Participants were asked to observe five blocks of 24 video clips each. Four blocks were associated with a specific emotion, namely, happiness, disgust, sadness, and fear. An additional block consisting of neutral video clips served as control. Video clips were edited color soundless film excerpts, each lasting ~9 s. They were selected and validated by Tettamanti et al., 2012. After each block, participants were asked to respond to an 8-items questionnaire by positioning a computer mouse on 0 (‘Not at all’) – 100 (‘Very much’) visuo-analogue scales (VAS). The emotional induction procedure was repeated three times, each corresponding to the ingestible pill position in the stomach (1) in the small (2) and in the large bowel (3).

© 2024, BioRender Inc. Figure 1 was created using BioRender, edited with Adobe Photoshop 7, and is published under a CC BY-NC-ND license. Further reproductions must adhere to the terms of this license.

Perceived emotions results (pill in the stomach, session 1).

Perceived emotions (disgust, fear, happiness, and sadness) measured using 0–100 visuo-analogue scale (VAS) ratings, as a function of the five categories of video clips (disgusting, fearful, happy, sad, and neutral) shown during the first session of this study (i.e., when the capsule was in the stomach). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. Significant differences refer to Bonferroni-corrected, Wilcoxon matched-pairs tests (threshold for multiple comparisons was set at 0.0125). ∧ p=0.013; * p≤0.01; ** p≤0.001.

Visceral sensations results (pill in the stomach, session 1).

Perceived visceral sensations (gastric, cardiac, and respiratory) and arousal, measured using 0–100 visuo-analogue scale (VAS) ratings, as a function of the five categories of video clips: disgusting, fearful, happy, sad, and neutral shown during the first session of this study (i.e. when the capsule was in the stomach). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. Significant differences refer to Bonferroni-corrected, Wilcoxon matched-pairs tests (threshold for multiple comparisons was set at 0.0125). ∧ p=0.018; * p≤0.01; ** p≤0.001.

Heart Rate (HR), Heart Rate Variability (RMSSD) and Spontaneous Eye Blinks results.

(A) Shows heart rate, as a function of the five categories of video clips: disgusting, fearful, happy, sad, and neutral shown during the first session of this study (i.e. when the capsule was in the stomach). * p≤0.01; ** p≤0.001. (B) Shows heart rate variability, indexed by RMSSD, as a function of the five categories of video clips: disgusting, fearful, happy, sad, and neutral shown during the first session of this study (i.e. when the capsule was in the stomach). * p≤0.05. (C) Shows the number of spontaneous eye blinks as a function of the five categories of video clips: disgusting, fearful, happy, sad, and neutral shown during the first session of this study (i.e. when the capsule was in the stomach). * p≤0.05; ** p≤0.01. Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively.

Association between the Stomach pH and perceived emotions (three-way interaction between item, stomach pH, and type of video-clip).

This figure illustrates the association between stomach pH and perceived emotions (disgust, fear, happiness, and sadness) across the five categories of video clips (disgusting, fearful, happy, neutral, and sad). Notably, it highlights the main differences, primarily observed in the left panel, concerning the disgusting video clips. Panel on the upper right highlights the main differences concerning the fearful video clips. Dots represent participants’ VAS ratings following the different types of video clip, shadows indicate Confidence Intervals. The pH has been mean-centred and scaled. *p≤0.05; ** p≤0.01.

Changes of stomach pH as function of type of video clip (left panel) and time, i.e. datapoints, (right panel).

*p≤0.05; ** p≤0.001.

Gastro-intestinal (GI) markers collected in the present study.

(A) Shows the SmartPill capsule used to record temperature, pH, and pressure of the gut and the intestine as well as a typical graph created by the dedicated MotiliGI software, plotting temperature (blue line), pH (green line), and pressure (orange bars) across the entire the GI tract. (B) Shows the device (PowerLab, ADInstruments Ltd) used to record electrogastrography (EGG) and a typical gastric myoelectric activity of a participant. The 1-channel bipolar electrode montage for the EGG recording is displayed on the left side of the figure.

© 2024, BioRender Inc. Figure 7 was created using BioRender, edited with Adobe Photoshop 7, and is published under a CC BY-NC-ND license. Further reproductions must adhere to the terms of this license.

Appendix 1—figure 1
Perceived emotions results (pill in the small bowel, session 2).

Perceived emotions (disgust, fear, happiness, and sadness) measured using 0–100 visuo-analogue scale (VAS) ratings, as a function of the five categories of video-clips (disgusting, fearful, happy, sad, and neutral) shown during the second session of this study (i.e. when the capsule was in the small bowel). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. * p≤0.05; ** p≤0.01.

Appendix 1—figure 2
Perceived emotions results (pill in the large bowel, session 3).

Perceived emotions (disgust, fear, happiness, and sadness) measured using 0–100 visuo-analogue scale (VAS) ratings, as a function of the five categories of video-clips (disgusting, fearful, happy, sad, and neutral) shown during the third session of this study (i.e. when the capsule was in the large bowel). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. * p≤0.05; ** p≤0.01.

Appendix 1—figure 3
Visceral sensations results (pill in the small bowel, session 2).

Perceived visceral sensations (gastric, cardiac, and respiratory) and arousal, measured using 0–100 visuo-analogue scale (VAS) ratings, as a function of the five categories of video-clips (disgusting, fearful, happy, sad, and neutral) shown during the second session of this study (i.e. when the capsule was in the small bowel). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. ^ p=0.019; * p≤0.01; ** p≤0.001.

Appendix 1—figure 4
Visceral sensations results (pill in the large bowel, session 3).

Perceived visceral sensations (gastric, cardiac and respiratory) and arousal, measured using 0–100 visuo-analogue scale (VAS) ratings, as a function of the five categories of video-clips: disgusting, fearful, happy, sad, and neutral shown during the third session of this study (i.e. when the capsule was in the large bowel). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. ^ p=0.018; * p≤0.05; ** p≤0.01.

Appendix 1—figure 5
Stomach pH influences perceived emotions (two-way interaction between item and gastric pH).

Effects of stomach pH on perceived emotions (disgust, fear, happiness, and sadness). * p≤0.05; ** p≤0.01.

Appendix 1—figure 6
Gastric cycle (tachigastric band) results.

Gastric cycle calculated in the tachigastric band as a function of the five categories of video-clips: disgusting, fearful, happy, sad, and neutral shown during the first session of this study (i.e., when the capsule was in the stomach). Boxplots are drawn from the first to the third quartiles, with the horizontal lines representing the medians. The lines extending from the top and bottom of the boxplots represent the smallest and largest values within 1.5 times the interquartile ranges (IQR) from the first and third quartiles, respectively. * p≤0.05.

Author response image 1

Tables

Table 1
Eight-item questionnaire.

English translation and original Italian text of the 8-items questionnaire probing the participants’ emotions, visceral feelings, and arousal after each block of video clips. Ratings were provided along 0–100 VAS scales.

ConstructCategoryItem (English)Item (Original language: Italian)
Emotional experiencePerceived disgustHow much disgust did you feel?Quanto disgusto hai provato?
Emotional experiencePerceived fearHow much fear did you feel?Quanta paura hai provato?
Emotional experiencePerceived happinessHow much happiness did you feel?Quanta felicità hai provato?
Emotional experiencePerceived sadnessHow much sadness did you feel?Quanta tristezza hai provato?
Visceral experiencePerceived gastric sensationsDid you feel retching, stomach contractions, stomach cramps or other gastro-intestinal sensations?Hai provato conati di vomito, contrazioni gastriche, crampi allo stomaco o altre sensazioni gastrointestinali?
Visceral experiencePerceived cardiac sensationsDid you feel your heart change (i.e. accelerate/slow down or beat)?Hai sentito il tuo cuore cambiare (accelerare/rallentare/ palpitare)?
Visceral experiencePerceived breathing sensationsDid you feel your breath change (heavy breath /holding breath/lack of air?)Hai sentito il tuo respiro cambiare (respirare affannosamente/trattenere il respiro/mancanza d’aria)?
ArousalPerceived arousalDid watching the clips bored/aroused you?Vedere i video ti ha annoiato/coinvolto?
Appendix 1—table 1
Results of Model 1 (pill in the stomach, session 1).

Perceived emotions predicted by the video clip content, type of item and stomach pH, temperature and pressure. Type III analysis of variance table with Satterthwaite’s method.

Sum SqMean SqNumDFDenDFF valuep
Video-clip content148643715.94460.3311.86903.475e-09***
Item124064135.23453.8413.20812.785e-08***
(Stomach) Pressure13211320.61286.714.21820.04090*
(Stomach) pH8079.7196.070.25450.61511
(Stomach) T314314.3131.691.00390.32397
Video-clip content:Item15460812884.012453.8441.1526<2.2e-16***
Video-clip content:(Stomach) Pressure918229.44477.110.73270.56993
Video-clip content:(Stomach) pH2335583.84471.881.86460.11549
Video-clip content:(Stomach) T1905476.34459.681.52150.19478
Item:(Stomach) Pressure1262420.63453.841.34330.25969
Item:(Stomach) pH77152571.73453.848.21422.470e-05***
Item:(Stomach) T1216405.33453.841.29460.27568
Video-clip content:item:(Stomach) Pressure4093341.112453.841.08950.36686
Video-clip content:item:(Stomach) pH7433619.412453.841.97840.02456*
Video-clip content:item:(Stomach) T2293191.012453.840.61020.83407
Appendix 1—table 2
Results of the Bonferroni corrected post hoc tests following the triple interaction Video-clip content*Item*Stomach pH of Model 1.

It has been performed, via emtrends function, following the significant triple interaction Video-clip content:item:(Stomach) pH, obtained by running the more conservative version of Model 1.

Video-clip contentItempHSEdfT ratiop
DisgustDisgust–15.645.75159.00–2.720.01 **
FearfulDisgust6.023.35152.001.800.07
HappyDisgust–2.182.87235.00–0.760.45
NeutralDisgust–1.685.17209.00–0.320.75
SadDisgust2.984.38191.000.680.50
DisgustHappy21.125.75159.003.67<0.001***
FearfulHappy7.563.35152.002.260.03*
HappyHappy5.942.87235.002.080.04*
NeutralHappy3.555.17209.000.690.49
SadHappy6.044.38191.001.380.17
DisgustSad–2.345.75159.00–0.410.68
FearfulSad1.813.35152.000.540.59
HappySad0.022.87235.000.010.99
NeutralSad–6.335.17209.00–1.220.22
SadSad4.684.38191.001.070.29
DisgustFear–10.905.75159.00–1.900.06
FearfulFear1.023.35152.000.310.76
HappyFear–0.402.87235.00–0.140.89
NeutralFear–0.985.17209.00–0.190.85
SadFear1.144.38191.000.260.80
Appendix 1—table 3
Results of Model 2 (pill in the stomach, session 1).

Stomach pH predicted by the video clip content and the time (i.e. number of datapoint). In this case all the datapoints collected via the Smartpill have been used. Type III analysis of variance table with Satterthwaite’s method.

Sum SqMean SqNumDFDenDFF valuep
Video-clip content25.52566.381446043.122.242<2.2e-16***
Time (datapoint)5.80595.805916043.220.2376.971e-06***
Video-clip content:Time (datapoint)3.72970.932446043.13.2500.01133*
Appendix 1—table 4
Results of the Bonferroni corrected post hoc tests following the double interaction Video-clip content*Item of Model 2.
Video-clip contenttrendSEdfT ratiop
Disgust–0.0015390.001216043–1.2690.2045
Fearful–0.0052080.001186043–4.421<0.0001
Happy0.0005280.0011860430.4470.6552
Neutral–0.0034020.001226043–2.7960.0052
Sad–0.0024630.001206043–2.0490.0405
Appendix 1—table 5
Results of Model 3 (EGG peak frequency_normogastric band, session 1).

Perceived emotions predicted by the video clip content, type of item and EGG normogastric peak frequency. Type III analysis of variance table with Satterthwaite’s method.

Sum SqMean SqNumDFDenDFF valuep
Video-clip content136173404.34418.8610.16607.302e-08***
Item81802726.63405.518.14222.819e-05***
Egg peak frequency466465.91402.481.39130.2389
Video-clip content:item14259911883.312405.5135.4858<2.2e-16***
Video-clip content:egg peak frequency823205.74425.150.61420.6526
Item:egg peak frequency522173.83405.510.51910.6693
Video-clip content:item:egg peak frequency2282190.212405.510.56790.8680
Appendix 1—table 6
Results of Model 5 (pill in the small bowel, session 2).

Perceived emotions predicted by the video clip content, type of item and small bowel pH, temperature and pressure. Type III analysis of variance table with Satterthwaite's method.

Sum SqMean SqNumDFDenDFF valueP
Video-clip content137783444.64478.8112.95855.013e-10***
Item33141104.63469.264.15540.006374**
(Small bowel) Pressure7877.71140.020.29230.589630
(Small bowel) pH805805.1169.103.02890.086244
(Small bowel) T4342.7130.060.16070.691327
Video-clip content:Item20827017355.812469.2665.2925<2.2e-16***
Video-clip content:(Small bowel) Pressure1003250.74486.530.94310.438650
Video-clip content:(Small bowel) pH778194.44477.460.73140.570808
Video-clip content:(Small bowel) T18145.44471.940.17070.953324
Item:(Small bowel) Pressure1160386.73469.261.45460.226235
Item:(Small bowel) pH610203.53469.260.76550.513789
Item:(Small bowel) T19665.23469.260.24520.864744
Video-clip content:item:(Small bowel) Pressure4598383.212469.261.44160.143390
Video-clip content:item:(Small bowel) pH1930160.812469.260.60500.838509
Video-clip content:item:(Small bowel) T5273439.412469.261.65300.074340
Appendix 1—table 7
Results of Model 6 (pill in the large bowel, session 3).

Perceived emotions predicted by the video clip content, type of item and large bowel pH, temperature and pressure. Type III analysis of variance table with Satterthwaite’s method.

Sum SqMean SqNumDFDenDFF valueP
Video-clip content141793544.74473.7511.35798.251e-09 ***
Item43191439.73468.864.61290.003418 **
(Large bowel) Pressure32.81269.210.00890.924857
(Large bowel) pH00.0158.500.00000.994501
(Large bowel) T3333.1131.270.10610.746856
Video-clip content:Item15902113251.812468.8642.4611< 2.2e-16 ***
Video-clip content:(Large bowel) Pressure1165291.24485.300.93310.444414
Video-clip content:(Large bowel) pH973243.44474.950.77980.538680
Video-clip content:(Large bowel) T720180.14472.930.57700.679421
Item:(Large bowel) Pressure343114.23468.860.36590.777669
Item:(Large bowel) pH755251.83468.840.80690.490491
Item:(Large bowel) T938312.63468.861.00170.391836
Video-clip content:item:(Large bowel) Pressure1496124.712468.860.39940.963735
Video-clip content:item:(Large bowel) pH2288190.712468.840.61090.833531
Video-clip content:item:(Large bowel) T2089174.112468.860.55780.875755
Appendix 1—table 8
Emotional video-clips content.

List of emotional video-clips used in the emotional induction task with a brief description in the second column, adapted by Tettamanti et al., 2012.

Category_Number of the Video-clipsDescription of the Video-clips
Disgust_1A monstrous creature vomits a corrosive fluid on a dead man’s face and dissolves it
Disgust_2A severed human head is covered with insects
Disgust_3A man is covered with faecal matter
Disgust_4Some dishes and a wall are covered with insects
Disgust_5A man takes a worm off an animal’s wound and holds it
Disgust_6A monstrous creature vomits a corrosive fluid on a dead man’s foot
Disgust_7A monstrous creature vomits a corrosive fluid on a dead man’s hand and dissolves it
Disgust_8A man plunges his hand in a toilet, retracts it covered with faecal matter and almost vomits
Disgust_9A man removes part of his own skin
Disgust_10A man vomits in a bowl, a man watches it and another man smells it
Disgust_11A man takes off his fingernail
Disgust_12A man eats snails
Disgust_13Close up on a fly which approaches a severed human hand covered with insects
Disgust_14Close up on insects
Disgust_15A man smells a bowl of vomit and drinks it
Disgust_16A girl vomits on a man’s face
Disgust_17A man squeezes a purulent dot on his hand
Disgust_18A man is covered with a substance and tries to remove it from his skin
Disgust_19Some surgeons perform a surgical operation on a bloodied inhuman creature
Disgust_20A monstrously shaped egg cracks open and viscous substances spill out
Disgust_21A bloodied girl whose upper lip is missing bites a man’s neck
Disgust_22A purulent inhuman organ is being dissected
Disgust_23A woman vomits on a man’s face
Disgust_24A monstrous creature is dissected
Fear_1A girl is approached by a scary creature
Fear_2A bear roars against a man
Fear_3A man attacks a woman
Fear_4A woman is approached by a monster
Fear_5Several men are falling from a mountain
Fear_6A woman is held underwater by a scary creature
Fear_7A woman tries to escape and she is stabbed in her hand
Fear_8A woman is attacked by a man
Fear_9A woman is attacked by a scary creature
Fear_10A man is attacked by a shark
Fear_11An aeroplane is disrupted during flight
Fear_12A woman is attacked by an alien
Fear_13A man is attacked by a shark
Fear_14A man is tied to a chair with his mouth duct taped
Fear_15Two climbers hang in the void
Fear_16A woman is attacked by a man
Fear_17A woman falls from a mountain
Fear_18A woman falls from a building
Fear_19A man is attacked by a man
Fear_20A man at risk of being crashed
Fear_21Two man hang on a building ledge
Fear_22A woman is approached by a monster
Fear_23A woman is attacked by a man
Fear_24A man is trapped underwater
Happy_1Several persons rejoice at a soccer match
Happy_2Several boys and a man rejoice after scoring a goal in a soccer match
Happy_3A woman smiles after seeing an old lady beating a young man with her purse
Happy_4A child smiles while looking at two persons smiling and hugging each other
Happy_5A woman smiles while looking at a man playing with a child
Happy_6A woman and a man kiss each other, women claps their hands
Happy_7A woman and a man run on a shore playing with each other
Happy_8A man rejoices after scoring a goal in a soccer match
Happy_9A woman and a man kiss each other
Happy_10A woman and a man kiss each other
Happy_11A woman and a man play together
Happy_12A man and a woman laugh together
Happy_13A man hugs a woman
Happy_14A man and a woman smile while looking at a dog lactating her puppies
Happy_15Several persons dance and a girl laughs
Happy_16A woman and a man laugh together
Happy_17A girl opens a present, a woman kisses her
Happy_18A man scores a goal in a soccer match
Happy_19A man hugs his sons
Happy_20A woman and a man dance and smile at each other
Happy_21Several persons rejoice at a soccer match
Happy_22Players celebrating for scoring a goal
Happy_23Several persons rejoice at a soccer match
Happy_24Several persons rejoice at a rugby match
Sad_1A woman cries and holds the hand of a man in a hospital bed
Sad_2A man cries while holding a dead woman
Sad_3Two persons are separated as the train leaves
Sad_4A sick child is in a hospital bed
Sad_5A man cries while holding a dead woman
Sad_6A woman kisses the forehead of a dead boy
Sad_7A woman cries on the phone
Sad_8A woman cries while holding a dead man
Sad_9Dead bodies are moved by the waves on the shore
Sad_10A man cries while holding the bloodied body of a man
Sad_11A woman cries and hugs a man
Sad_12A sick woman is in bed, a man holds her hand
Sad_13A man crying while looking at a dead man
Sad_14A woman cries, two women hug her
Sad_15A man holds a dead man
Sad_16Several dead bodies lay upon the ground
Sad_17Several persons are in a hospital bed
Sad_18Dead bodies lay on a shore
Sad_19Several persons watch three coffins on the ground
Sad_20A woman and a man hold each other
Sad_21Three persons cry while holding each other
Sad_22A man looks upon a dead body
Sad_23A woman closes herself in a room and cries
Sad_24A woman lays a flower on a coffin at a funeral, another woman watches
Neutral_1Two men, one speaking and the other one listening
Neutral_2A woman opening the window of the dog kennel in an old mansion
Neutral_3A woman meets a man at the train station
Neutral_4A woman takes the computer from a bag and puts it on a table
Neutral_5Several persons observe drawings and sculptures
Neutral_6Several persons talk and walk in an office
Neutral_7A woman walks in a large building, several other persons in the background
Neutral_8Two waiters greet several persons entering a room
Neutral_9A man closes the door and walks away
Neutral_10A man works in a building site, several other men working in the background
Neutral_11A woman in a boat sits and opens a book
Neutral_12Several persons walking in a corridor, a woman enters an office
Neutral_13Men carving and moving large cinematographic props
Neutral_14A woman and a man speak while cleaning the kitchen
Neutral_15A woman walks down the road, some children on bikes wave at her
Neutral_16A women’s meeting, one speaks while the others nod
Neutral_17A woman hoovers a room
Neutral_18A man walks in the countryside while reading
Neutral_19A man writes while sitting on the outside of a ferry
Neutral_20Different scenes from a food market
Neutral_21A woman types at the computer and lifts the receiver
Neutral_22A man and two young men talk by the phone
Neutral_23A man drawing
Neutral_24A man cleans the leaves off the yard
Author response table 1
Type III Analysis of Variance Table with Satterthwaite's method.
Sum SqSum SqNumDFDenDF F valuePr(>F)
district1509.5754.742 1681.49023< 2.2e-16 ***
Author response table 2
anova(Stomach_VASvalence,type=3,ddf="Satterthwaite") Type III Analysis of Variance Table with Satterthwaite's method.
Sum SqMean SqNumDFDenDFF valuePr(>F)
valence1207312072.71507.4423.64861.545e-06 ***
item4348714495.83502.1528.3949< 2.2e-16 ***
zpressure832832.51414.531.63070.20232
zpH15851585.01191.593.10470.07911
zT12771276.61107.392.50070.11673
valence:item6990723302.43502.1545.6456< 2.2e-16***
valence: zpressure253252.61520.360.49470.48213
valence:zpH762761.91508.951.49250.22240
valence:zT691690.91506.451.35340.24523
item:zpressure1810603.53502.151.18210.31596
item:zpH1736578.73502.151.13360.33493
item:zT375125.03502.150.24480.86503
valence: zpressure2025675.13502.151.32250.26627
valence:zpH13043.53502.150.08520.96814
valence:zT20066.73502.150.13070.94183

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  1. Giuseppina Porciello
  2. Alessandro Monti
  3. Maria Serena Panasiti
  4. Salvatore Maria Aglioti
(2024)
Ingestible pills reveal gastric correlates of emotions
eLife 13:e85567.
https://doi.org/10.7554/eLife.85567