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Biological Psychology xxx (2012) xxx–xxx

1

Letter to the Editor

2

Accuracy and awareness of perception: Related, yet distinct

Q1 (commentary on Herbert et al., 2012)

3 The finding of Herbert and colleagues (2012) in the January 4 issue of Biological Psychology sheds interesting new perspectives

5 on the correspondence between homeostatic challenges and

accu-6 racy of heartbeat perception. One of their conclusions is that 7 changes in autonomic activity, which in their study were induced 8 by short-term fasting, intensify overall Interoceptive Awareness 9 (IAw). Below, it is argued that this conclusion can be somewhat 10 misleading; a more nuanced conclusion and additional directions 11 for future research based on this revised conclusion are proposed. 12 In the article of Herbert and colleagues as well as in numer-13 ous other articles, heartbeat perception tasks are considered to 14 be a proxy of IAw. To say that “cardiac IAw [. . .] reflects the sen-15 sory accuracy of perceiving one’s own cardiac signals” (p.77, Herbert 16 et al., 2012) is to say that IAw and Interoceptive Accuracy (IAc) are 17 synonymous, whereas in fact they are not. IAc specifically refers 18 to the capability of accurately perceiving changes in homeostatic 19 function. To be aware, means to be cognizant, to be mindful. Thus 20 IAw should be taken to mean the cognizant, mindful perception of 21 bodily signals (given the definition of interoception proposed by

22 Herbert and colleagues). Although IAw can be accompanied by an

23 accurate perception of bodily sensations, such accuracy is not nec-24 essarily implied. This distinction between awareness and accuracy 25 is highlighted by a study of Khalsa and colleagues (2008) who found 26 that IAw is increased in meditative practices, but IAc is not. 27 Nevertheless, the idea that IAw and IAc can be used inter-28 changeably is widespread, and most prevalent in the heartbeat 29 perception literature (e.g., Stewart et al., 2001; Sturges and Goetsch, 30 1996). This practice likely stems from the interoceptive sensitiv- 31 ity hypothesis (Ehlers and Breuer, 1992; Tyrer, 1973), which states 32 that high anxious persons and panic disorder (PD) patients (condi-33 tions associated with high IAw) have a more accurate perception 34 of bodily sensations. Of the numerous studies that found results 35 supporting the interoceptive sensitivity hypothesis, all barring no 36 exception, used heartbeat perception tasks (e.g., Critchley et al., 37 2004; Ludwickrosenthal and Neufeld, 1985; Richards et al., 2003; 38 Schandry, 1981; Zoellner and Craske, 1999). On the other hand, 39 studies looking at the accuracy of perception of non-cardiac inter-40 oceptive signals such as respiration, found that individuals with 41 high negative affectivity – a trait associated with higher IAw (Stegen 42 et al., 2001), as well as with anxiety and PD – are less accurate 43 perceivers under negative affective conditions than are controls 44 (Bogaerts et al., 2005; van den Bergh et al., 2004), which is contra- 45 dictory to the interoceptive sensitivity hypothesis. Such findings 46 are indicative that (1) IAw and IAc are indeed two distinct con-47 cepts, and (2) that good accuracy on heartbeat perception tasks 48 does not necessarily translate to accurate perception of other bodily

49 processes.

The arguments above illustrate that considering heartbeat per- 50

ception tasks as a measure of overall IAw, or of overall IAc, is to 51

discard all the necessary nuance regarding interoception. Although 52

heartbeat perception tasks are a measure of one type of IAc, 53

interoceptive sensations are heterogeneous in nature. As a result, 54

accuracy of heartbeat perception cannot simply be assumed to cor- 55

relate with accurate perception of other interoceptive sensations 56

such as gastro-intestinal or respiratory sensations. Unfortunately, 57

standardized tasks measuring non-cardiovascular types of IAc are 58

currently far and few between: such tasks should receive more 59

attention in future research. 60

Of additional importance is that intra-individual changes in per- 61

formance on the heartbeat perception task in the study of Herbert 62 et al. (2012) followed an increase in inotropic cardiac activity. This 63

could be indicative that not all homeostatic challenges that alter 64

cardiac activity, may lead to an increased accuracy of heartbeat 65

perception. E.g., it can be argued that homeostatic challenges which 66

lead to a decrease in inotropic activity, perhaps lead to a decreased 67

accuracy of heartbeat perception, because discriminatory feedback 68

of overlying somatic tissues is reduced. Given that accurate percep- 69

tion of heartbeat can occur solely through somatic afferents from 70

tissue overlying the heart region, or solely through visceral affer- 71

ents (Khalsa et al., 2009), it is of importance to understand whether 72

intra-individual changes in accuracy of heartbeat perception are 73

specifically associated with either of both somatic or visceral affer- 74

ents. 75

In conclusion, we would like to more accurately rephrase the 76

summarizing remark of Herbert and colleagues, as this has impor- 77

tant implications for interpretation of all interoception related 78

studies as well as for future directions for their own and other’s 79

research. Their results indicate that homeostatic challenges which 80

lead to an increase in inotropic cardiac activity, lead to an increased 81

accuracy of heartbeat perception and perhaps increased awareness 82

of heartbeats, but there is no conclusive evidence that they lead to 83

an increase of other types of IAc, nor to an increase of overall IAw. 84

It is unclear whether homeostatic challenges leading to a decrease 85

in inotropic activity, lead to changes in accuracy of heartbeat per- 86

ception. 87

Based on this, further studies should be designed to under- 88

stand whether the improvements in accuracy on the heartbeat 89

perception task only follow homeostatic challenges which increase 90

inotropic cardiac activity, or whether they also follow challenges 91

which decrease inotropic cardiac activity. Additionally, it may be 92

relevant to anesthetize somatic tissue overlying the heart as has 93

been done in the study of Khalsa et al. (2009), in order to clarify Q3 94

whether the increases in performances of accuracy are specifically 95

due to somatic or visceral afferents. The most important message 96

is that we need to acknowledge the distinction between awareness 97

and accuracy of perception, and that we need to remain careful 98

in extrapolating conclusions based solely on heartbeat perception 99

0301-0511/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.biopsycho.2012.09.012

Please cite this article in press as: Ceunen, E., et al., Accuracy and awareness of perception: Related, yet distinct (commentary on Herbert et al., 2012). Biol. Psychol. (2012), http://dx.doi.org/10.1016/j.biopsycho.2012.09.012

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Contents lists available at SciVerse ScienceDirect

Biological Psychology

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2 Letter to the Editor / Biological Psychology xxx (2012) xxx–xxx

100 101

tasks as if they are representative of other types of IAc or of general

IAw. van den Bergh, O., Winters, W., Devriese, S., van Diest, I., Vos, G., de Peuter, S.,

133

2004. Accuracy of respiratory symptom perception in persons with high and 134

low negative affectivity. Psychology & Health 19 (2), 213–222. 135

103 104

Bogaerts, K., Notebaert, K., Van Diest, I., Devriese, S., De Peuter, S., Van den Bergh,

O., 2005. Accuracy of respiratory symptom perception in different affective con- Erik Ceunen∗ 1 Q2 138

105 texts. Journal of Psychosomatic Research 58 (6), 537–543. Ilse Van Diest 139

106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132

Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A., Dolan, R.J., 2004. Neural systems supporting interoceptive awareness. Nature Neuroscience 7 (2), 189–195. Ehlers, A., Breuer, P., 1992. Increased cardiac awareness in panic disorder. Journal of

Abnormal Psychology 101 (3), 371–382.

Herbert, B.M., Herbert, C., Pollatos, O., Weimer, K., Enck, P., Sauer, H., et al., 2012. Effects of shortterm food deprivation on interoceptive awareness, feelings and autonomic cardiac activity. Biological Psychology 89 (1), 71–79.

Khalsa, S.S., Rudrauf, D., Damasio, A.R., Davidson, R.J., Lutz, A., Tranel, D., 2008. Interoceptive awareness in experienced meditators. Psychophysiology 45 (4), 671–677.

Khalsa, S.S., Rudrauf, D., Feinstein, J.S., Tranel, D., 2009. The pathways of interoceptive awareness. Nature Neuroscience 12 (12), 1494–1496.

Ludwickrosenthal, R., Neufeld, R.W.J., 1985. Heart beat interoception – a study of

individual-differences. International Journal of Psychophysiology 3 (1), 57–65.

Richards, J.C., Cooper, A.J., Winkelman, J.H., 2003. Interoceptive accuracy in nonclin- ical panic. Cancer Treatment and Research 27 (4), 447–461.

Schandry, R., 1981. Heart beat perception and emotional experience. Psychophysi- ology 18 (4), 483–488.

Stegen, K., Van Diest, I., Van de Woestijne, K.P., Van den Bergh, O., 2001. Do persons with negative affect have an attentional bias to bodily sensations? Cognition & Emotion 15 (6), 813–829.

Stewart, S.H., Buffett-Jerrott, S.E., Kokaram, R., 2001. Heartbeat awareness and heart rate reactivity in anxiety sensitivity: a further investigation. Journal of Anxiety Disorders 15 (6), 535–553.

Sturges, L.V., Goetsch, V.L., 1996. Psychophysiological reactivity and heartbeat awareness in anxiety sensitivity. Journal of Anxiety Disorders 10 (4), 283–294. Tyrer, P.J., 1973. Relevance of bodily feelings in emotion. Lancet 1 (7809),

915–916.

University of Leuven, Department of Psychology and 140 Educational Sciences, Research Group on Health 141 Psychology, P.O. Box 3726, 3000 Leuven, Belgium 142 Johan Vlaeyena,b,2 143 a University of Leuven, Department of Psychology and 144

Educational Sciences, Research Group on Health 145

Psychology, P.O. Box 3726, 3000 Leuven, Belgium 146

b Maastricht University, Department of Clinical 147

Psychological Science, P.O. Box 616, 6200 MD 148

Maastricht, The Netherlands 149

Corresponding author. Tel.: +32 16325874. 150 E-mail addresses: Erik.Ceunen@ppw.kuleuven.be (E. 151

Ceunen), Ilse.VanDiest@ppw.kuleuven.be (I. Van 152

Diest), Johan.Vlaeyen@ppw.kuleuven.be (J. 153 Vlaeyen) 154 1 Tel.: +32 16326029; fax: +32 16325923. 155 2 Tel.: +32 16325915/+31 433881047; fax: +32 156 16326144. 157 Available online xxx 158

Please cite this article in press as: Ceunen, E., et al., Accuracy and awareness of perception: Related, yet distinct (commentary on Herbert et al., 2012). Biol. Psychol. (2012), http://dx.doi.org/10.1016/j.biopsycho.2012.09.012

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Zoellner, L.A., Craske, M.G., 1999. Interoceptive accuracy and panic. Behaviour 136

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