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Modulation of the startle reflex by pleasant and unpleasant music

International Journal of Psychophysiology 71 (2009) 37–42 Contents lists available at International Journal of Psychophysiology Modulation of the startle reflex by pleasant and unpleasant music Mathieu Roy, Jean-Philippe Mailhot, Nathalie Gosselin, Sébastien Paquette, Isabelle Peretz Department of Psychology, BRAMS, University of Montreal, Canada Available online 23 July 2008 The issue of emotional feelings to music is the object of a classic debate in music psychology. Emotivistsargue that emotions are really felt in response to music, whereas cognitivists believe that music is only representative of emotions. Psychophysiological recordings of emotional feelings to music might help to resolve the debate, but past studies have failed to show clear and consistent differences between musical excerpts of different emotional valence. Here, we compared the effects of pleasant and unpleasant musical Startle reflexZygomatic excerpts on the startle eye blink reflex and associated body markers (such as the corrugator and zygomatic activity, skin conductance level and heart rate). The startle eye blink amplitude was larger and its latency was shorter during unpleasant compared with pleasant music, suggesting that the defensive emotional system was indeed modulated by music. Corrugator activity was also enhanced during unpleasant music, whereasskin conductance level was higher for pleasant excerpts. The startle reflex was the response that contributedthe most in distinguishing pleasant and unpleasant music. Taken together, these results provide strongevidence that emotions were felt in response to music, supporting the emotivist stance.
2008 Elsevier B.V. All rights reserved.
techniques that are independent of voluntary subject control, such aspsychophysiological measures. Following this line of research, The emotional power of music remains a mystery. Unlike most compared the autonomic responses elicited by different emotional inducers, music is not a sentient being nor does it seem to musical emotions and found that sad, happy, and fearful music could have any obvious adaptive value (Yet, most people be differentiated by their autonomic activation patterns: Sad music affirm that they feel strong emotions when they listen to music was most strongly associated with changes in heart rate, blood ). This paradox led many music scholars to pressure, skin conductance and skin temperature, fearful music was believe that music is only iconic or representative of emotion, a mostly associated with changes in the rate and amplitude of blood position coined as ‘cognitivist' by . Opponents to this view, flow, and happy music principally produced changes in respiratory known as ‘emotivists', feel that the cognitivist position does not activity and showed the highest skin conductance level (SCL).
render justice to the direct and unmediated fashion in which emotions However, subsequent studies have failed to replicate many of these are experienced by listeners (Although the debate is at a findings. found that skin conductance responses theoretical level, its resolution has practical implications for inter- (SCR) were highest during the listening of fearful music, preting music effects. Indeed, if music is only representative of observed increased SCL during sad and fearful music emotion, its therapeutic value could be seriously questioned. Studies compared to happy music, and found higher SCL measuring physiological, endocrine and brain responses to music as during the listening of unpleasant compared to pleasant music.
indices of emotional reactivity have supported the emotivist view, but Moreover, found higher heart rates during the nature of these emotional responses and their resemblance with unpleasant compared to pleasant music, whereas emotions induced by other stimuli is unclear.
, and found theopposite. Therefore, there are inconsistent findings of the intensity and 1.1. Autonomic nervous system responses direction of these autonomic responses between studies.
Such inconsistencies across psychophysiological emotion studies In order to show that people not only recognize but feel emotions are relatively common ), and the outcomes may in response to music, emotional reactions should be measured by be related to some context-bound patterns of actions that allow thesame emotion to be associated with a wide range of behavior andvarying patterns of somatovisceral activation ().
⁎ Corresponding author. Université de Montréal, Département de psychologie, However, it should be noted that some psychophysiological measures Pavillon Marie-Victorin, local D-418, 90 av. Vincent d'Indy, Montréal, QC, Canada H2V appear more reliable than others. For example, respiration rate appears E-mail address: (I. Peretz).
to be consistently higher during happy and fearful music than during 0167-8760/$ – see front matter 2008 Elsevier B.V. All rights reserved.
doi: M. Roy et al. / International Journal of Psychophysiology 71 (2009) 37–42 brain activations alone do not allow for the distinction between ), although this effect may reflect differences processes involved in emotional perception and emotional feeling.
in arousal that differentiate happiness and fear from sadness, and not Physiological changes that affect the body and its responses are musical emotions per se Indeed, cognitive necessary to demonstrate the induction of emotional feelings.
theories of emotion have criticised the use of autonomic measures asindexes of felt emotions due to the non-specific nature of arousal 1.4. Present study (For example, high arousal characterizesboth fear and happiness. Moreover, in music, arousal is known to be Although these studies demonstrate that some emotions are felt in mainly driven by its tempo ). The fact that response to music, the results do not definitely refute the cognitivist respiration rate has been linked to tempo through what appears to be a viewpoint, as many psychophysiological responses are inconsistent, general entrainment mechanism further contributes to discredit and the responses that appear to induce the most stable responses respiration rate as a clear index of musical emotions ( (e.g., respiration rate or hormonal responses) may be influenced by ). Although tempo is one of the main determinants of musical other confounding factors, such as arousal or distraction. Finally, brain emotions, musical emotions depend on many other factors than simple imaging techniques cannot solely discriminate emotional feelings tempo perception Thus, until the context-bound from other aspects of emotional processing.
patterns of action that affect the autonomic responses to musical In order to demonstrate the induction of emotional feelings, emotions understood and controlled, more specific measures of involuntary changes that affect the body and emotional processing emotional reactions to music are needed to convince the sceptical have to be observed in response to musical excerpts conveying dif- cognitivist that music effectively induces emotions in the listener.
ferent emotions. In this context, the startle reflex is a good candidatemeasure, as it has been extensively and successfully used to probe 1.2. Hormonal responses emotional reactions. It is an automatic defensive reaction to surprisingstimuli and can be measured by the magnitude of the eye blink Neuroendocrine and hormonal responses constitute yet another triggered by a loud white noise. As a response of the defensive type of involuntary response that can be linked to emotional feelings.
emotional system, it is frequently used to test the efficacy of anxiolytic Contrary to physiological responses, some hormones can be more drugs ) or to explore emotional reactivity in readily associated with positive or negative emotion (), affective disorders (). In normal individuals, it is such as cortisol with stress and negative emotions, or immunoglobin typically enhanced by negative emotions and diminished by positive A (S-IgA) with relaxation and positive emotions ones, using pictures films or ). A few studies have found that listening to relaxing and pleasant sounds () to induce emotions. The present music was associated with lower levels of cortisol study applied an affective startle modulation paradigm to musical lower plasmatic levels of β-endorphins stimuli and compared the effects of pleasant and unpleasant musical (and higher mu-opiate receptor expression excerpts on the acoustic startle blink reflex. If emotions are induced (However, those studies only compared music during music listening, then the startle reflex should be larger and of with a silent control condition. Therefore, the observed effect may be shorter latency during unpleasant music compared to pleasant music.
attributed to non-emotional aspects of the musical condition, such as Moreover, in order to measure music effects on emotional distraction. Indeed, when two musical conditions are compared, no reactions, heart rate and skin conductance responses were also differences were found between music inducing positive or negative obtained along with facial expressions by assessing electromyographic moods on levels of cortisol ), nor between up- or (EMG) activity of the zygomaticus major (smiling) and the corrugator down-lifting musical excerpts on levels of S-Iga, dopamine, norepine- supercilii (frowning). Previous studies have shown that the activity of phrenine, epinephrine or number of lymphocites these muscles discriminated well between pleasant and unpleasant suggesting that the differences previously observed emotions elicited by pictures (Thus, it was expected were mainly related to non-specific aspects of the task. One exception that zygomatic activity would be higher during pleasant music, and is the study by , who observed higher levels of β- corrugator activity to be more noticeable during unpleasant music endorphins, adrenocorticotropic hormone (ACTH), cortisol, norepi- nephrine and growth hormone in youngsters listening to techno-music compared to classical music. However, these changes in neuroendocrine responses appeared to be mainly linked to the higharousal induced by the techno-music, combined with the novelty- 2.1. Participants seeking temperament of the participants. Neuroendocrine responses,although promising, appear to have the same limitations as autonomic Sixteen participants (9F, 7M), aged between 20 and 40 years (M = 25.1 ± 9.3 years) took part in this study. None were musicians, allreported fewer than five years of musical training, and none claimed 1.3. Brain imaging any regular practice of a musical instrument.
Brain imaging techniques provide yet another way to measure 2.2. Musical excerpts emotional reactions objectively. Studies using such techniques haveshown that pleasant emotional reactions to music activate regions The musical excerpts used in this study were adapted from a prior previously known to be involved in approach-related behaviors, such study on pain modulation Three 100 s excerpts of as the prefrontal cortex pleasant music and three 100 s excerpts of unpleasant music were ), periacqueductal gray selected from a pool of 30 musical excerpts. Each of the 30 excerpts had matter and the nucleus accumbens been previously evaluated by 20 independent participants on the Negative emotions in dimensions of valence (on a 0 = ‘pleasant' and 9=‘unpleasant') and contrast activate regions involved in withdrawal-related behavior, arousal (with 0 = ‘relaxing' and 9=‘stimulating'). Three highly pleasant such as the parahippocampal gyrus (and amygdala and three highly unpleasant excerpts were selected. Since unpleasant (). Although these observations are fairly excerpts were always judged to be arousing, all excerpts were selected in consistent with activations observed with other emotional inducers, the high range of arousal. Pleasant excerpts were judged to be more

M. Roy et al. / International Journal of Psychophysiology 71 (2009) 37–42 pleasant than unpleasant excerpts (mean valence for pleasant averaged for each subject and musical condition. Facial EMG was excerpts = 2.40, mean valence for unpleasant excerpts = 6.68; t(19)= recorded over the left corrugator and zygomatic sites 5.58, p b 0.05) and did not differ in arousal (mean arousal for pleasant using 8 mm Ag/AgCl shielded electrodes. Signals excerpts = 5.00, mean arousal for unpleasant excerpts = 5.18; t (19)= were bandpass filtered from 90 Hz to 1000 Hz and transformed using 1.535, n.s.). The selected pleasant excerpts were taken from the classical the root mean square. Sampling rate was set at 1000 Hz. Area under or jazz/pop repertoire and could be described as uplifting, with a rather the curve of the rectified EMG signal were then extracted for the fast tempo, such as the "Opening of William Tell" by Rossini. Unpleasant corrugator and zygomatic muscle.
excerpts were mainly taken from the contemporary music repertoire.
Electrocardiogram (ECG) was recorded using a standard 3 lead Examples of excerpts for each emotion category can be heard on our web montage (Einthoven lead 2 configuration) (Biopac EL503). Instanta- site at All selections were normalized neous intervals between each R-wave of the ECG (RRI) were calculated to equate loudness across musical excerpts by setting the peaks of the from the ECG using a peak detection algorithm to detect successive R- excerpts at 8% of the maximum volume allowed, using the normalisation waves and obtain a continuous R–R tachogram. Careful examination of option of the Cool Edit 2 sound editing software.
the ECG and the tachogram ensured that the automatic R-wave The primary emotions (sadness, happiness, fear, anger, peacefulness detection procedure had been performed correctly.
and surprise) and moods (anger, depression, fatigue, anxiety, vigor and Skin conductance level (SCL) was recorded on the palmar surface of confusion, as measured with the "profile of mood states", POMS; the left hand, at the thenar and hypothenar eminences ), induced by those excerpts were also previously assessed ). The signal was smoothed and the mean SCL was calculated for ). Results showed that the primary emotions conveyed the whole duration of each musical excerpt and averaged for the by the excerpts were consistent with their emotional valence. Pleasant pleasant and unpleasant music condition.
excerpts were associated with happiness whereas unpleasant ones wereassociated with fear and anger. Results on the mood questionnaire confirmed these observations: The subscales for highly arousingnegative moods, such as anger and anxiety, were higher after listening The physiological sensors were affixed while the participants sat to the unpleasant excerpts, whereas the subscales for less arousing comfortably in a quiet room. The pleasant and unpleasant excerpts moods, such as depression, remained unaffected. Thus, the selected were presented in a counterbalanced order across participants. excerpts convey primary emotions and induce moods consistent with illustrates the procedure for one musical excerpt. Each musical excerpt their positive or negative valence and their high level of arousal.
started with an emotional induction period of 21.3 s in which therewere no startle probes. The remaining 78.7 s were divided in six 11 s 2.3. Data collection and reduction time window in which a startle probe occurred randomly. Each timewindow was separated by a period of 2.3 s in which no startle probe Startle responses were elicited by a 100 dB SPL, 50 ms burst of occurred. After each musical excerpt, the subject rated his/her white noise, with instantaneous rise time. The acoustic startle probe emotional reaction to the music on the dimensions of valence was presented over Sony MDR-v200 headphones. The eye blink (0 = unpleasant, 9 = pleasant) and arousal (0 = relaxing, 9 = stimulating).
component of the startle reflex was recorded electromyographicallyfrom the orbicularis oculi muscle beneath the left eye, using two 2.5. Data analysis miniature 4 mm Ag/AgCl shielded electrodes placed 1.5 cm apart and asignal ground electrode placed on the forehead, following the The musical excerpts were assessed statistically for the expected guidelines of . The signal was amplified by emotional effects by comparing the mean ratings of valence and 1000 and band-pass filtered at 90 Hz–500 Hz using a Biopac MP150 arousal. Sound intensity was assessed before each startle probe in both System (Biopac Systems, Inc., Santa Barbara, CA). The sampling rate musical conditions using RMS power preceding each startle probe for was set at 1000 Hz. The amplified signal was then transformed using the pleasant and unpleasant music conditions. After these control the root mean square.
analyses, a multivariate analysis of variance (MANOVA) was conducted The maximum amplitude and latency of each startle response were to test for the effects of emotional condition (pleasant or unpleasant) extracted from the data. Following the guidelines of on the means of all the physiological measures used (startle blink reflex , only responses for which the onset occurred between 21 and amplitude and latency, corrugator and zygomatic activity, RRI and SCL).
120 ms from noise onset were considered as startle responses and The MANOVA was followed by separate t-tests for each physiological included in the analysis. The raw blink measurements were then measure. Finally, a discriminant function analysis was conducted to standardised within each subject to decrease variability due to test if some patterns of physiological activation could reliably differences in the absolute size of the startle blink across subjects, discriminate between the pleasant and unpleasant musical conditions.
and expressed as T scores (50 + 10z), which yielded a mean of 50 and astandard deviation of 10 for each subject. The blink amplitudes and latencies T scores were then averaged for the pleasant and unpleasantmusic condition.
3.1. Self-reported emotions To assess the sound intensity of the musical excerpts prior to each startle probe, the total root mean square amplitude (RMS) power was The mean valence and arousal ratings were calculated for the extracted for 1 s windows preceding each burst of white noise and pleasant and unpleasant excerpts. The t-tests performed on these Fig. 1. Distribution of startle probes during one musical excerpt. Participants listened passively to music for 21.3 s. In the last 78.7 s of the excerpts, six startle probes were randomlydelivered within 11 tie windows separated by periods of 2.3 s during which no probe could occur.

M. Roy et al. / International Journal of Psychophysiology 71 (2009) 37–42 average ratings confirmed that the intended emotions of the musical excerpts were well recognized. The pleasant and unpleasant excerpts Canonical variate correlation coefficients for the discriminant function differed significantly on the dimension of valence (with a mean rating Startle amplitude of 8.49 and 1.91, respectively; t (15) = 13.04, p b 0.001). In contrast, pleasant and unpleasant musical excerpts did not differ on the Corrugator activity dimension of arousal (with a mean rating of 6.41 and 7.50, respectively; Zygomatic activity Skin conductance level t (15) = 1.79, n.s.).
3.2. Sound amplitude condition (t (15) = 2.43, p b 0.05, η2 = 0.28). The physiological responses The RMS power of the 1 s windows preceding each startle probe were not limited to the 21.3 initial seconds without startle probes but was equivalent for the pleasant (23.03 ± 0.68) and unpleasant (23.21 ± were considered for the whole excerpt instead because only non- 0.49) musical excerpts (t (15) = 0.31, n.s.).
significant trends in the same direction were obtained on the initialpart of the musical excerpts.
3.3. Physiological measures 3.4. Discriminant analysis illustrates the mean values of each physiological measure for the pleasant and unpleasant music condition. The results of the The results of the discriminant analysis showed that the pleasant MANOVA showed that the physiological responses were significantly and unpleasant excerpts could easily be differentiated by a single affected by the musical condition (F (6, 10) = 6.86, p b 0.01, η2 = 0.81).
function (Wilk's lambda (6) = 0.51, p b 0.01). This function correctly The startle blink reflex was larger (t(15) = 3.35, p b 0.01, η2 = 0.43) and classified pleasant excerpts in 75% of cases and unpleasant excerpts in faster (t (15) = 2.81, p b 0.05, η2 = 0.35) during the unpleasant music as 87.5% of cases. summarizes the canonical variate correlation compared to the pleasant music. Activity of the corrugator muscle was coefficients of each physiological variable for the discriminant higher during the unpleasant condition (t (15) = 2.79, p b 0.05, η2 = function. These canonical variate correlation coefficients were much 0.34), but no significant difference in the activity of the zygomatic more important for startle amplitude and latency compared to the muscle was obtained between the two musical conditions (t (15) = other physiological measures, indicating that the startle reflex was the 1.35, n.s., η2 = 0.11). RRI was also not affected by the valence of the measure that contributed the most to the separation of the musical musical excerpts (t (15) = 0.72, n.s., η2 = 0.03). In contrast, the SCL was conditions. Although there is a lack of consensus regarding how high found to be larger during the pleasant than the unpleasant music correlations in a loading matrix should be interpreted, typically only Fig. 2. Mean physiological responses for the pleasant and unpleasant musical conditions. Error bar represents one standard error above the mean. Significant differences (p b0.05) areindicated by asterisks. Note that error bars reflect the between-subjects variance in each condition whereas the results of the statistical tests reflect the within-subject contrast acrossexperimental conditions.
M. Roy et al. / International Journal of Psychophysiology 71 (2009) 37–42 variables with loadings of .32 and above are considered interpretable.
shown to be significantly modulated by the valence of the excerpt.
suggest that loadings over 0.71 are considered This lack of sensitivity for zygomatic compared to corrugator activity excellent, 0.63, very good, 0.55, good, 0.45, fair and 0.32, poor. In is a common finding (perhaps because the light of those guidelines, the canonical variates coefficients appear zygomatic is implicated in some negative emotions such as disgust or excellent for the startle reflex, but difficult to interpret for the other that it is involved with display rules and other fine voluntary motor Skin conductance, while having little contribution to the discrimi- nant function, proved to be higher during the pleasant compared to theunpleasant excerpts. This finding adds to the controversy surrounding 4.1. Induction of emotional feelings by music the interpretation of skin conductance changes in response to musicalemotion. The present findings are consistent with those of The startle reflex was of higher amplitude and shorter latency but inconsistent with and during the listening of unpleasant in comparison with pleasant . Moreover, the present findings are opposite to those generally excerpts, suggesting that different emotional states were effectively observed with other emotional induction techniques such as mental induced by music. As the musical excerpts were manipulated to vary imagery or the presentation of emotional movie clips for which SCL is on the dimension of valence independently of arousal or loudness, the higher during negatively valenced emotion This observed effects are likely to reflect the induction of positive and outcome suggests that skin conductance levels might be related to negative emotional states in response to music, thereby supporting some aspects of the emotional response that are not directly linked to the emotivist's stance in contrast to critiques of cognitivists. First, the the perceived valence and arousal and may vary from one study to startle reflex is an involuntary response that does not depend on the another. In the present case, the pleasant and arousing excerpts might doubtful capacity of the subjects to adequately describe their own have prompted motoric activity such as dancing or tapping of the foot.
experience. Second, the affective startle modulation effect is a reliable Finally, no differences in heart rate were found between pleasant and measure that avoids the important variability characterizing auto- unpleasant excerpts. Taken together with the negative findings of nomic nervous system measures. Moreover, startle modulation can be and this lack of difference ascribed to the emotional valence rather than arousal or attention, suggests that heart rate alone is not sufficient to differentiate pleasant thereby contrasting with prior studies. Third, because the modulation from unpleasant musical conditions.
of the startle reflex indicates facilitation or inhibition of a motivationalpropensity to withdraw, it convincingly distinguishes the induction of 4.3. Implications emotional states from the cold perception of emotional features. Thus,music appears to be as powerful as pictures (), films The present study supports the emotivist stance and provides or natural sounds to some theoretical justifications for the use of music as a therapy. If induce positive and negative emotions.
music is able to induce emotions that can reduce the activity of the The absence of a neutral control condition complicates the emotional defensive system, it can be used to alleviate some unpleas- comparisons with studies using different inducers of emotion, since ant emotional states, such as anxiety (), depression it is difficult to tell if the startle modulation was due to an increase of or pain (). In addition, the the reflex during unpleasant music, a decrease of the reflex during demonstration that emotions are indeed felt in response to music pleasant music, or a combination of both. The absence of a neutral also opens up questions about how and why it does so. The control condition, however, was not incidental as it is difficult to find combination of psychophysiological recordings with brain imaging "neutral" music as judged by a majority of listeners. In addition, the techniques, in addition to self-reported measures of emotion and use of a silent control condition would not have been informative as careful manipulation of the musical stimuli, will help to characterize sound level by itself has been shown to influence the acoustic startle how the brain and the body interact to create emotional feelings to ). Similarly, white noise matched with the musical excerpts for sound amplitude could not have been a better controlcondition because white noise is generally experienced as unpleasant.
Nonetheless, a study using a similar design in which three startleprobes were delivered within 2-min long video clips, showed that The work was supported by a grant from the Natural Science and pleasant videos reduced the magnitude of the startle reflex compared Engineering Research Council of Canada (NSERC) to Isabelle Peretz, to neutral videos, whereas unpleasant ones increased it ( and by a doctoral scholarship from the NSERC to Mathieu Roy. We Hence, it is reasonable to assume that the present results thank Amee Baird for English editing, Francine Giroux for statistical depend on the effect of a combination of both facilitation and advice and Pierre Rainville for his suggestions on physiological signal inhibition of the defensive system. Nevertheless, the fact that the startle reflex was modulated by the emotional valence of the excerptsis sufficient to attest that emotional states were induced by music.
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Scottish Intercollegiate Guidelines NetworkPart of NHS Quality Improvement Scotland Autism spectrum disordersBooklet for parents and carers We would like to thank all the young people who took part in the focus groups to provide us with their ideas and illustrations for this booklet. © Scottish Intercollegiate Guidelines Network ISBN 978 1 905813 27 8