2022年度日本認知科学会第39回大会

O3-003A: fMRI
Awareness of cardiac/gastric interoception andits individual differences modulate the neural dynamics
1, 2, *

1

1

Yusuke Haruki, Keisuke Suzuki, and Kenji Ogawa
1

2

Hokkaido University, Japan Society for the Promotion of Science*haruki@let.hokudai.ac.jp

Abstract

interoception suggests that the insular cortex, particularly the

Senses that arise from within the body are referred to asinteroception. Empirical studies on interoception haveprimarily utilized cardiac sensation (senses related to one’s
heartbeat) because of its easiness of measuring non-invasively.
With this practice, however, it is unclear whether
interoception is a unimodal sensory phenomenon. Here, weshow that the different types of phenomenal interoception
evoke a particular pattern of neural activities. Specifically,
attention on cardiac and gastric (related to the stomach)interoception activated different brain regions and altered thefunctional connectivity in these regions. Furthermore,individual differences in cardiac/gastric sensitivity wereassociated with intrinsic functional connectivity of the insularcortex. Submodalities of interoception would be distinctive intheir neural dynamics as well as phenomenal experience.

right anterior insula, plays critical role in generating
phenomenal interoception [3]. This idea has been supported
by fMRI studies using cardiac interoception [4, 5]. However,given the variety of phenomenal interoception, we consider
that the opinion could be suspicious without a directcomparison of brain activity between cardiac and other typesof interoception. Several fMRI studies have already usedgastric (senses related to stomach sensation) and urinary(related to bladder) interoception to capture the neural basis ofinteroception [6, 7], but none of them compared the neuralactivation by the types of interoception.
Here, we directly compared neural activation during

Keywords ― interoception, fMRI, functional connectivity

cardiac and gastric interoception to test whether the different

1.

types of phenomenal interoception evoke particular pattern ofIntroduction
Interoception refers to senses that arise from within thebrain activation. In addition to differences in activation, webody. For example, hunger, heartbeat sensations, dizziness,

also focused on temporal dynamics (functional connectivity)urination, fever, and many other phenomenal experiences are

between the brain regions during cardiac/gastric interoception.

subject to interoception. Empirical studies on interoception,

Furthermore, we assessed individual differences in cardiac

however, have been unable to incorporate such diversity due

and gastric sensitivity and tried to associate it with the intrinsic,

to the difficulty of measuring and manipulating bodily signals.

task-free functional connectivity in the insular cortex.

Awareness of cardiac signals has been extensively used toThrough a series of analyses, we showed that the brain

investigate the characteristics of interoception. Behavioral

dynamics underlying cardiac and gastric interoception largely

tasks on heartbeat perception (e.g., counting own heartbeat)differ, highlighting the importance of submodalities ofhave revealed a large individual difference in cardiac

interoception.

interoception (or its sensitivity) [1]. Although those tasks havebeen widely used and well-validated, cardiac sensitivity does2.

Materials and Methods

not necessarily correspond to bodily awareness in broader

2.1.

fMRI experiments

sense. Subjective sensibility to interoception measured via

A total of 30 healthy volunteers (12 women, 21.61 ± 2.45

questionnaire and cardiac sensitivity usually do not correlate

years old) participated in the experiment on two occasions, atwith each other [1]. Another study has shown that a meditation

least a week apart. On day 1, we asked participants topractitioner does not have sensitive cardiac interoception [2].

experience fMRI scanning to obtain brain activation during

One seminal opinion regarding the neural substrates ofrest and performing tasks. Participants first underwent a five-57

2022年度日本認知科学会第39回大会

O3-003A

minute resting-state fMRI scan in which they looked at a

(Welcome

Department

ofCognitive

Neurology,

fixation crossbar with their eyes open and did not think

http://www.fil.ion.ucl.ac.uk/spm). The standard procedure ofanything in particular.

preprocessing (realignment, normalization to Montreal

Subsequently, we asked participants to perform an

Numerological Institute (MNI) space, and smoothing with 6

interoceptive attention task in the scanner [6, 7], which was

mm cube Gaussian kernel) was performed before statisticalmodified for our purposes. The task had three conditions:

inference. A high-pass filter was applied with a cutoff of 128

HEART (related to cardiac), STOMACH (related to gastric),s, and serial correlations among scans were estimated using an

and VISUAL (control). In each condition, participants tried toautoregressive model to exclude signal noise.

perceive sensations from the instructed source (i.e., heart,

Individual level generalized linear model included eachstomach, and slight color change of words) by directing theirtask trial block as separate box-car regressors that wereattention. There were five trials for each condition per run,convolved with the canonical hemodynamic responsewith five runs repetition (a total of 125 scans per condition).

function. To reduce motion-related artifacts, six motion

All scans were performed on a Siemens 3-Tesla Prisma

parameters were included as nuisance regressors.

scanner (Erlangen, Germany) with a 64-channel head coil at

We then performed three group analyses: random effects

Hokkaido University. The scanning parameters for functional

analysistodirectlycomparebrain

activation,

data were as follows: repetition time, 2,000 ms; field of view,

psychophysiological interaction analysis to compare the

192 × 192 mm; matrix, 94 × 94; 32 axial slices; and slicechanges in functional connectivity, and correlation analysis

thickness, 3.500 mm with a 0.875-mm gap. Thus, the voxel

for the resting-state fMRI data. First, we performed one

size was 2.042 × 2.042 × 4.375 mm.

sample t-test on random effects using the contrast images ofthe HEART and STOMACH conditions. By doing so, we

2.2.

Behavioral experiments

identified brain regions selectively activated for cardiac and

On day 2, we asked participants to complete a heartbeat

gastric interoception across the whole brain. These detailed

counting task [1, 8] and water load test [9] out of the MRI

results and further discussion are now available as a preprint

scanner to assess individual differences in cardiac and gastric[10].

sensitivity behaviorally. The heartbeat counting task required

Subsequently, we defined the region of interest (ROI) for

participants to silently count the number of their heartbeats inthe second analysis based on the results of the first analysis. A

a certain period by focusing on the internal bodily sensation.

4 mm sphere ROI centering on the peak activated coordinates

Estimating the number and taking pulse outside the body wasin the first analysis for each condition was created for the mostprohibited. We evaluated individual sensitivity of cardiac

activated four clusters. This resulted in four individual ROIs:

interoception by comparing the counted number to the actual

the left orbitofrontal (center coordinate: x, y, z) = (-42, 26, -number of heartbeats. The calculation yielded a score ranging

16), left primary visual (-12, -73, -13), right anterior insula (33,from 0 to 1, with 1 indicating the highest sensitivity.

17, 2), and the left primary motor area (-48, -7, 29). Thereafter,

In the water load test, participants were asked to drink room

we tested whether the attentional focus on the heart/stomachtemperature, non-carbonated water ad libitum using a straw

modulates the functional connectivity. We performed aand to stop drinking when they first felt the sign of subjective

psychophysiological interaction analysis that models the task

fullness. A total of 1.5 liters of water was filled in a five-liter

type (cardiac and gastric), the time course of ROI activity, andcapacity container whose contents were invisible from thethe interaction between them. This analysis can estimate task-

outside; thus, participants did not know the water volume they

dependent changes in functional connectivity between the

consumed. The difference between the total volume and

ROI and the other brain regions. The effect of cardiac andconsumed volume was used as an estimation of individual

gastric interoception on the functional connectivity wassensitivity of gastric interoception.

computed for each ROI for each participant. Finally, as agroup level analysis, we performed one sample t-tests on these

2.3.

fMRI data analysis

individual level results.

All image processing was performed using SPM12

The third analysis was independent of the first and second

58

2022年度日本認知科学会第39回大会

O3-003A

ones. Here, we identified the brain regions that exhibited an

activated in gastric interoception showed decreased, rather

enhanced intrinsic (task-free) functional connectivity with thethan increased, functional connectivity with other regions

structural subdivisions of the insular cortex in people withduring gastric interoception compared to cardiac interoception.

high cardiac/gastric sensitivity. We adopted the ROIs from theMore specifically, the left primary visual seed showed

Hammersmith atlas [11]: the right middle short gyrus for thedecreased

anterior insula and the anterior long gyrus for the posterior

occipitotemporal, left temporoparietal, and right frontal

insula. The selection was based on previous findings that theregions. The functional connectivity between the left

middle short gyrus was the most activated when people

orbitofrontal seed and right frontal/temporal regions also

focused on their heartbeats [12] and that the anterior longdecreased in gastric interoception. The left primary motor

gyrus corresponds to the primary interoceptive cortex that isseed had decreased connectivity with the medial occipitalfirst projected with visceral signals at the cortical level [13].

regions. In the same line, the right anterior insula seed that was

Individual correlation maps were generated by extracting themore activated during cardiac interoception exhibitedtime series signal in each ROI (i.e., the right anterior anddecreased functional connectivity with the right primaryposterior insula) and calculating correlation coefficients withvisual area related to gastric interoception. Only the left

the signals of each voxel throughout the whole brain. We also

primary visual seed showed enhanced functional connectivity

modeled the individual cardiac and gastric sensitivity that waswith the contralateral primary visual area in gastricmeasured via the behavioral experiments as group levelinteroception.

functional

connectivity

with

the

right

covariates of interest. We tested the group level effects of

We also found that individual differences in cardiac andcardiac/gastric sensitivity on the intrinsic functional

gastric sensitivity were differently associated with the intrinsic

connectivity by performing one sample t-tests.

(task-free) functional connectivity in the insula (Figure 3). In
people with higher cardiac sensitivity, the right primary

3.

Results

interoceptive cortex (posterior insula) showed a stronger

3.1.

Behavioral result

intrinsic functional connectivity with the bilateral frontal

The mean score of cardiac sensitivity measured by theoperculum, temporoparietal junction, left frontal pole, and left

heartbeat counting task was 0.43 ± 0.25 while the averageinferior frontal gyrus but decreased connectivity with thevolume left in the bottle in the water load test was 1179 ±bilateral dorsolateral prefrontal cortex and superior parietal

189.54 ml. Pearson’s correlation coefficient between the twolobule. Such people also had the increased intrinsic

did not reject the null hypothesis that the coefficient was zeroconnectivity of the right anterior insula with the bilateral(r = 0.24, t28 = 1.31, p = .20).

ventromedial prefrontal cortex and right temporoparietal
junction but decreased with the right middle insula.

3.2.

fMRI result

Conversely, higher gastric sensitivity contributed to stronger

We report all the results surviving peak level threshold p

intrinsic connectivity of the right dorsal posterior insula with< .001 (uncorrected) and cluster level threshold 15 < k. Firstly,

the bilateral putamen and left thalamus. The right anterior

we found that cardiac interoception enhanced the neuralinsula was more connected with the bilateral temporoparietal

activation in the right anterior insula compared to gastricjunctioninpeoplewithhighergastric

sensitivity.

interoception. In contrast, the activated regions in the gastriccontrasted to cardiac interoception encompassed the larger
brain areas, including the visual area, sensorimotor region,
hippocampus, superior frontal and orbitofrontal cortex(Figure 1).
The functionally defined ROI seeds showed alteredfunctional connectivity with other brain regions depending on
Figure 1. Selectively activated brain regions for cardiac andgastric interoception. z denotes the axial slice in MNI space.
ROIs in yellow were used in the psychophysiologicalthe task type (focusing on cardiac or gastric interoception)(Figure 2). Interestingly, the functional seed regions more592022年度日本認知科学会第39回大会

O3-003A

interaction analysis. L: left hemispherecortex with other brain regions was associated with individual
differences in cardiac/gastric sensitivity measured via
behavioral tasks. These results reveal that the different typesof phenomenal interoception are associated with particularneural dynamics in the human brain, suggesting thatinteroception is not a unimodal sensory experience even at theneural level.
A previous meta-analysis on fMRI studies using cardiac
interoception identified the consistently activated brain
regions in the right insula and supplementary motor area [14].
These results strongly supported the dominance of the rightinsula in interoception [3, 4, 5]. However, the present study

Figure 2. Results of the psychophysiological interaction
analysis. Colored regions showed altered functional
connectivity in the seed regions defined in Figure 1.
depending on the attentional focus (cardiac, hot; gastric,cold). AI, anterior insula; FC, functional connectivity; M1,
primary motor area; OFC, orbitofrontal cortex; V1, primaryvisual area

showed gastric interoception activated a widespread region
across the sensorimotor region and frontal region in gastricinteroception, while cardiac interoception enhanced theactivation in the right insula. Therefore, the role of the rightinsula for interoception may be cardiac-specific rather thaninteroception in general.
Moreover, we found task-modulation effects on functional
connectivity in the brain regions that were selectively
activated during cardiac/gastric interoception. In general,
functional connectivity in these functionally defined seedregions reduced during gastric compared to cardiac
interoception. The results show that gastric contrasted to
cardiac interoception evoked enhanced activation over
distributed brain areas, but they were functionallydisconnected from other brain regions.
It is interesting to note that gastric interoception showedenhanced but functionally disconnected activations in the
primary visual and sensorimotor area. It appears puzzling thatbrain activation in the primary sensory cortex differed
between conditions because any visual or sensorimotor
signals were absent in the present interoception task. This
could be explained by differences in the functional roles ofeach phenomenal interoception [10]. For example, thefunctional role of gastric interoception has been proposed to

Figure 3. Subdivisions of the insula showing alteredintrinsic functional connectivity depending on individual
difference in cardiac/gastric sensitivity. FC, functional
connectivity

modulate feeding and foraging behavior in which agents must
properly regulate their sensorimotor ability [15]. In line with
this, it could be reasoned that gastric interoception that is4.

Discussion

likely to occur during food intake may be more relevant to the

In this study, we show that focusing on cardiac and gastricvisual and sensorimotor regions than cardiac interoception.

interoception activated different brain regions and altered their

Furthermore, individual differences in intrinsic functional

functional connectivity depending on the task type. Moreover,connectivity in the right anterior and posterior insula were

intrinsic (task-free) functional connectivity in the insularassociated with interoceptive sensitivity. Particularly, higher

60

2022年度日本認知科学会第39回大会

O3-003A[5] Tan, Y., Wei, D., Zhang, M., Yang, J., Jelinčić, V., & Qiu, J.
(2018). “The role of mid-insula in the relationship between
cardiac interoceptive attention and anxiety: evidence from an
fMRI study”, Scientific Reports, 8(1), 17280.
[6] Simmons, W. K., Avery, J. A., Barcalow, J. C., Bodurka, J.,
Drevets, W. C., & Bellgowan, P. (2013). “Keeping the body inmind: Insula functional organization and functional connectivity
integrate interoceptive, exteroceptive, and emotionalawareness”, Human Brain Mapping, 34(11), 2944–2958.
[7] Deville, D. C., Kuplicki, R., Stewart, J. L., Paulus, M. P., Khalsa,
S. S., Aupperle, R. L., Bodurka, J., Cha, Y. H., Feinstein, J.,
Savitz, J. B., & Victor, T. A. (2020). “Diminished responses tobodily threat and blunted interoception in suicide attempters”,
eLife, 9, e51593.
[8] Schandry, R. (1981). “Heart Beat Perception and Emotional
Experience”, Psychophysiology, 18(4), 483–488.
[9] Herbert, B. M., Muth, E. R., Pollatos, O., & Herbert, C. (2012).
“Interoception across modalities: On the relationship between
cardiac awareness and the sensitivity for gastric functions”,
PLoS ONE, 7(5), e36646.
[10] Haruki, Y., & Ogawa, K. (March 11, 2022). “Cardiac and gastricinteroception have distinct neural substrates”, bioRxiv[11] Faillenot, I., Heckemann, R. A., Frot, M., & Hammers, A. (2017).
“Macroanatomy and 3D probabilistic atlas of the human insula”,
NeuroImage, 150, 88–98.
[12] Haruki, Y., & Ogawa, K. (2021). “Role of anatomical insular
subdivisions in interoception: Interoceptive attention andaccuracy have dissociable substrates”, European Journal of
Neuroscience, 53(8), 2669–2680.
[13] Evrard, H. C. (2019). “The organization of the primate insularcortex”, Frontiers in Neuroanatomy, 13, 00043.
[14] Schulz, S. M. (2016). “Neural correlates of heart-focusedinteroception : a functional magnetic resonance imaging metaanalysis”, Philosophical Transactions of the Royal Society B:
Biological Sciences, 371.
[15] Kanoski, S. E., & Grill, H. J. (2017). “Hippocampus
Contributions to Food Intake Control: Mnemonic,
Neuroanatomical, and Endocrine Mechanisms”, BiologicalPsychiatry, 81(9), 748–756.
[16] Ainley, V., Apps, M. A. J., Fotopoulou, A., & Tsakiris, M. (2016).
““Bodily precision”: A predictive coding account of individual
differences in interoceptive accuracy”, PhilosophicalTransactions of the Royal Society B: Biological Sciences, 371.

sensitivity in cardiac interoception contributed to theincreased connectivity in both the anterior and posterior insulawith the frontal and temporal regions. Sensitive cardiac
interoception was also characterized by the decreased
connectivity in the posterior insula with the superior parietal
region and the anterior insula with the ipsilateral middle insula.
In contrast, high gastric sensitivity enhanced the intrinsic
functional connectivity in the anterior insula with the bilateral
temporoparietal junction and in the posterior insula with theputamen. Together, the functional connectivity between theright anterior insula and temporoparietal junction may benecessary for sensitive interoception over modalities.
However, cardiac sensitivity may require the (de)coupling of
the insula with the regions orienting attention (the superiorparietal and frontal regions) compared to gastric interoception.
This result would be in line with the proposal that cardiac
sensitivity would be enhanced via attentional modulation of
sensory gain of the heartbeat-related signals [16].
The present results indicated that the neural dynamics
underlying cardiac and gastric interoception differed greatly.
Although the previous discussion on interoception has
depended primarily on studies using cardiac interoception
alone, researchers need to consider that interoception has
submodalities and some results in a certain modality do notcoincide with others. In future studies, the functional roles ofdifferent phenomenal interoception in relation to one’s
behavior, cognition, and emotion would be of interest.

Acknowledgement
This work was supported by JSPS, KAKENHI Grant Number
20K20423 to K.O. and 22J20351 to Y.H, and by JST, CREST
Grant Number JPMJCR21P4 to K.S. and.

References[1] Garfinkel, S. N., Seth, A. K., Barrett, A. B., Suzuki, K., &Critchley, H. D. (2015). “Knowing your own heart:
Distinguishing interoceptive accuracy from interoceptive
awareness”, Biological Psychology, 104, 65–74.
[2] Khalsa, S. S., Rudrauf, D., Hassanpour, M. S., Davidson, R. J.,
Tranel, D., & Davidson, R. J. (2020). “The practice of
meditation is not associated with improved interoceptive
awareness of the heartbeat”, Psychophysiology, 57, e13479.
[3] Craig, A. D. (2009). “How do you feel — now? The anterior
insula and human awareness”, Nature Reviews Neuroscience,10(1), 59–70.
[4] Critchley, H. D., Wiens, S., Rotshtein, P., Öhman, A., & Dolan,
R. J. (2004). “Neural systems supporting interoceptive
awareness”, Nature Neuroscience, 7(2), 189–195.

61