Interoceptive inference: homeostasis and

TICS-1302; No. of Pages 2
Letter
Interoceptive inference: homeostasis and
decision-making
Xiaosi Gu1,2 and Thomas H.B. FitzGerald1
1
2
The Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, WC1N 3BG, UK
Virginia Tech Carilion Research Institute, 2 Riverside Circle, Roanoke, VA 24016, USA
In a recent article in TICS [1], Seth makes the compelling
claim that interoceptive inference (i.e., the approximate
Bayesian inference about internal bodily states) underlies
body ownership and selfhood. In this letter, we argue that
the significance of interoceptive inference extends beyond
this. In particular, we emphasise the role of interoceptive
inference in both homeostasis and allostasis (i.e., the process of achieving homeostasis) [2], and how this role
grounds decision-making and motivated behaviour, when
contextualised in the setting of hierarchical active inference.
To persist over time, organisms must restrict themselves to a small subset of possible biophysical states [3].
Under the free energy principle [3], this homeostasis arises
because organisms minimise surprise, conditioned on their
model of the world. In other words, they seek out the states
they expect to occupy, where these ‘familiar’ states are
innately valuable [3]. There are two ways to achieve this:
first, through homoeostatic control of the internal milieu of
the agent via autonomic responses [1,4,5]; and, second,
through allostatic actions on the external world [2,3]
(Figure 1). Consider an agent whose blood sugar level falls
below a certain threshold to an undesirable or surprising
level. In this situation, homeostasis can be maintained
through the metabolism of bodily fat stores (when food
is not available), or consummatory behaviour (when food is
available). In real-life situations, both autonomic reflexes
and somatic reflexes conspire to maintain homeostasis.
Crucially, both processes can also be explained as surprise
or prediction-error minimisation, albeit acting through
different mechanisms. We argue that interoceptive inference is not only involved in the first (homeostatic) process,
but also participates in the latter (allostatic) process by
informing value-based choices about the internal state of
the body.
We believe this notion can explain the key role of the
insular cortex in decision-making [6]. A popular taxonomy
considers the representation of internal and external
states as a prelude to decision-making, followed by valuation, action selection, outcome evaluation, and, finally,
learning and information updating [7]. The insular cortex
is widely held to encode and represent interoceptive information [1,4,5] and, in so doing, acts to contextualise choice
behaviour by informing other neural systems about the
internal state of the body. In other words, the insula
computes a ‘state’ variable of the internal world of the
agent and passes it to other neural systems that carry out
other computations in decision-making.
Naturally, this perspective also enables us to sketch a
potential relation between the insula and the ventromedial
prefrontal cortex (vmPFC), a region crucial for valuation
[8,9]. The vmPFC receives both interoceptive and exteroceptive information and is strongly coupled to the hippocampus, giving it access to mnemonic information and
model-based planning [9]. This anatomical affiliation
enables it to integrate interoceptive information conveyed
by the insula with exteroceptive, and other types of information, to generate amodal value representations that
Current
Expected
X
Allostasis
World
Homeostasis
Body
TRENDS in Cognitive Sciences
Corresponding authors: Gu, X. ([email protected]);
FitzGerald, T.H.B. ([email protected]).
1364-6613/$ – see front matter
ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tics.2014.02.001
Figure 1. Illustration of the role of interoceptive inference in homeostasis and
decision-making. A change in x, one of internal states of the body, away from an
expected (unsurprising) bodily state is registered by the insular cortex. (Black:
inferred current value. Green: expected value. Broken lines: full probability
distribution. Unbroken lines: mean.) This deviation or surprise can be reduced
either homeostatically, via autonomic reflexes that resolve interoceptive prediction
errors, or allostatically, via action, giving rise to motivated behaviour that resolves
proprioceptive prediction errors.
Trends in Cognitive Sciences xx (2014) 1–2
1
TICS-1302; No. of Pages 2
Letter
drive choice behaviour or prescribe behaviour through
proprioceptive predictions. This picture corresponds closely with a wide consensus as to the role of the vmPFC [8].
To conclude, we extend the notion of interoceptive
inference to cover (allostatic) exteroceptive and proprioceptive decision-making processes. We propose that, in
addition to representing body ownership and selfhood
[1], the contribution of interoceptive inference also involves
maintaining homeostasis by informing allostatic decisions
about the internal state of an agent. Proposing a key role
for interoception in decision-making is not new [1,4,5,10],
and our proposal can be seen as placing ideas such as the
‘somatic marker hypothesis’ [10] within embodied predictive coding. However, our formal hypothesis enables us to
make more specific predictions about the functional role of
the insula and other brain regions. From this perspective,
the links between value, homeostasis, and interoceptive
inference can be disclosed within the larger setting of
hierarchical active inference.
Acknowledgements
We thank Prof. Read Montague for providing funding for X.G. through a
Wellcome Trust Principle Fellowship Award, Prof. Ray Dolan for
providing funding for T.H.B.F. through Wellcome Trust Senior Investigator Award 098362/Z/12/Z, and Karl Friston, Read Montague, and Ray
2
Trends in Cognitive Sciences xxx xxxx, Vol. xxx, No. x
Dolan for helpful discussions. The Wellcome Trust Centre for Neuroimaging is supported by core funding from the Wellcome Trust 091593/Z/10/Z.
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