Bolus isoproterenol infusions provide a reliable method for assessing
interoceptive awareness
S.S. Khalsa
a,c,
⁎
, D. Rudrauf
a
, C. Sandesara
b
, B. Olshansky
b
, D. Tranel
a
a
Department of Neurology (Division of Behavioral Neurology and Cognitive Neuroscience) and Neuroscience Program, University of Iowa, United States
b
Department of Internal Medicine (Division of Cardiology), University of Iowa, United States
c
Medical Scientist Training Program, University of Iowa, United States
abstractarticle info
Article history:
Received 26 October 2007
Accepted 4 August 2008
Available online 27 September 2008
Keywords:
Interoception
Isoproterenol
Emotion
Heartbeat detection
Respiration
Interoception, defined as the perception of internal body states, plays a central role in classic and contemporary
theories of emotion. In particular, deviations from baseline body states have been hypothesized to be integral to
the experience of emotion and feeling. Consequently, reliable measurement of interoception is critical to the
testing of emotion theories. Heartbeat perception tasks have been considered the standard method for
assessing interoceptive awareness, primarily due to their non-invasive nature and technical feasibility.
However, these tasks are limited by the fact that above chance group performance rates on heartbeat detection
(or the frequency of ‘good detectors’) are rarely higher than 40%, meaning that such tasks (as they are typically
utilized) do not obtain a measure of interoceptive awareness in the majority of individuals. Here we describe a
novel protocol for inducing and assessing a range of deviations in body states via bolus infusions of
isoproterenol, a non-selective beta adrenergic agonist. Using a randomized, double-blinded, and placebo-
controlled experimental design, we found that bolus isoproterenol infusions elicited rapid and transient
increases in heart rate and concomitant ratings of heartbeat and breathing sensations, in a dose-dependent
manner. Our protocol revealed changes in interoceptive awareness in all 15 participants tested, thus
overcoming a major limitation of heartbeat detection tasks. These findings indicate that bolus isoproterenol
infusions provide a reliable method for assessing interoceptive awareness, which sets a foundation for further
investigation of the role of interoceptive sensations in the experience of emotion.
© 2008 Elsevier B.V. All rights reserved.
1. Introduction
1.1. Background
Interoceptive sensations occupy a central role in classic and
contemporary theories of emotion. In The Expression of Emotion in
Man and Animals, Charles Darwin (1872) highlighted the involvement
of sensations from the viscera in his description of the experience of
fear, noting “the heart beats quickly and violently, so that it palpitates
or knocks against the ribs” and that “in connection with the disturbed
action of the heart the breathing is hurried.” The subsequent highly
influential James–Lange theory of emotion, put forth independently
by William James (1884) and Carl Lange (1885), posits that signals
originating from the within the body, such as the sensation of the
heartbeat and breath, are fundamental for the experience of emotion
to the extent that “the feeling of bodily changes as they occur IS the
emotion,” and that in the absence of the experience of bodily change
all that is left is a “cold and neutral state of intellectual perception”
(James, 1884). Since the inception of the James–Lange theory, the role
of afferent bodily sensation in emotion has been debated. Against the
James–Lange “peripherist” theory, Walter Cannon (1927, 1929) and
Philip Bard (1928) defended a “centralist” theory of emotion, arguing
that the full range of visceral sensations was neither a necessary nor a
sufficient condition for the experience of emotion. This was based on
observations of intact emotional expression in deafferented cats,
intact emotional experience in humans with spinal cord transections,
and the absence of genuine reports of emotional experience in
humans following sympathetic modulation of visceral sensations with
adrenaline (Marañon, 1924). Stanley Schacter and Jerome Singer
endorsed a similar view in their “attribution theory” (Reisenzein,
1983; Schacter and Singer, 1962), based on studies of epinephrine
injections in humans. The theory stated that the subjective perception
of physiological arousal, although often a component of the
experience of emotion, was not sufficient to elicit specific emotional
states. Emotions required an additional cognitive process of attribu-
tion of meaning to the perceived physiological response, based on
available contextual cues.
Contemporary views continue to highlight the importance of
peripheral sensations in the subjective experience of emotion. Beyond
International Journal of Psychophysiology 72 (2009) 34–45
⁎ Corresponding author. Neuroscience Graduate Program, Department of Neurology,
University of Iowa, 200 Hawkins Drive, Iowa City, IA 52242, United States. Tel.: +1 319
335 8303; fax: +1 319 384 7199.
E-mail address: sahib-khalsa@uiowa.edu (S.S. Khalsa).
0167-8760/$ – see front matter © 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijpsycho.2008.08.010
Contents lists available at ScienceDirect
International Journal of Psychophysiology
journal homepage: www.elsevier.com/locate/ijpsycho