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Brain networks underlying the retrieval and experience of music-evoked autobiographical memories. P. Janata* & S.T. Tomic. Center for Mind and Brain, Univ. of California, Davis, Davis, CA. 365.27 Introduction The evocation of autobiographical memories and associated emotions by music counts among the most poignant experiences associated with music. Accordingly, excerpts of music can serve as potent retrieval cues with which to study the functional architecture of autobiographical memory. Converging evidence (Figure 1) suggests that the rostral aspect of the medial prefrontal cortex (BA10) is a region where music and autobiographical memories might be integrated. This study tested the hypothesis that experiencing autobiographically salient musical excerpts would result in increased activation in the medial prefrontal cortex. Methods Prescreening and memory characterization As part of an ongoing survey and description of autobiographical memories evoked by pieces of music, subjects heard 30s excerpts that were selected at random from the Billboard Top 100 Pop and R&B charts from the years in which the subject was between 7 and 19 years of age. Following each excerpt, a subject reported whether the song was familiar and if so whether it evoked a weakly or strongly autobiographical memory or no clear memory at all. For songs identified as autobiographically salient, a more extensive set of questions was administered to probe the specific content of the evoked memory/ies. Subjects were invited to participate in the fMRI version of the experiment if >30% of the excerpts evoked an autobiographical memory. fMRI experiment 14 subjects (12 female) were presented with 30 stimuli (selected according to the same criteria as above) across two scanning runs. Excerpts encountered by the subject in the prescreen were excluded from selection. One minute of resting-state activity was recorded prior to the 1st stimulus. Following each excerpt, subjects provided ratings (using left hand) of the affective valence (5-point scale) and arousal (5-pt scale) they experienced while listening to the excerpt, their familiarity with the song (2 pt scale), its autobiographical salience (3 pt scale), and the orientation of their attention toward the memories (5 pt scale) and music (5 pt scale). Immediately following the scanning session, subjects completed a detailed survey about their episodic memories pertaining to songs they correctly identified as having heard in the scanner and flagged as being autobiographically salient. Scanner parameters: Siemens 3T Trio, 34 slices (4 mm thick, 0 skip), TR=2.0s, in-plane resolution: 3.4x3.4 mm. Data were spatially normalized and analyzed in SPM5. See Fig. 4 for examples of subject design matrices. correlation matrix 05lrl85061 06lra87031 -20 -10 +0 +10 +20 +30 +40 +50 +60 05gza86261 -20 -10 +0 +10 +20 +30 +40 +50 +60 -20 -10 +0 +10 +20 +30 +40 +50 +60 -20 -10 +0 +10 +20 +30 +40 +50 +60 -20 -10 +0 +10 +20 +30 +40 +50 +60 -20 -10 +0 +10 +20 +30 +40 +50 +60 Music playing Individual subject data Design Matrices Autobiographical salience 4 6 8 10 12 -12 -10 -8 -6 -4 t-values (p<0.001) activation deactivation music playing autobiographical salience responses valence motion Time music playing autobiographical salience responses valence motion Time 0 0.05 0.1 0.15 0.2 0.25 0.3 Strongly Disagree Disagree Disagree Somewhat Neither Agree nor Disagree Agree Somewhat Agree Strongly Agree The song evokes an emotional reaction 0 0.1 0.2 0.3 0.4 Not At All Very Little Somewhat Fairly Strongly Very Strongly The emotion is experienced ... average proportion of autobiographical stimuli 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 Happy Calm Proud Content Loved Optimistic Inspired Excited Innocent Energized Strong Joyous Spiritual Reverent Hopeful Bittersweet Rejected Chills Youthful Sad Angry Embarrassed Upset Depressed Regretful Nostalgic Confused Jittery Lonely Homesick Jealous Repulsed Guilty Naive Other Associated emotions average proportion of stimuli w/associated emotion 0 20 40 60 80 100 0 20 40 60 80 #subjects % of all stims Autobiographical association 0 20 40 60 80 100 0 20 40 60 80 #subjects % of autobiographical stims Specific time in life 0 20 40 60 80 100 0 20 40 60 80 #subjects % of autobiographical stims Specific person 0 20 40 60 80 100 0 20 40 60 80 #subjects % of autobiographical stims Emotional association N=310 Figure 4. Design matrices and activation maps for 3 individual subjects. The 30s presentations of songs are denoted in the design matrices by the white bars in the “music playing” regressors. The set of regressors la- belled “responses” includes both the response cues and responses following each stimulus. The “autobiographi- cal salience” regressor codes a parametric modulation of the stimulus presentation epoch, with an unfamiliar song assuming a value of -1, a weakly autobiographical song a value of 0, and a strongly autobiographical song a value of +1. Valence is coded similarly, with “somewhat” and “strongly” displeasing ratings being coded with -1, neutral ratings with 0, and somewhat and strongly pleasing ratings with +1. Activation maps show regions of significant (p<0.001 unc.) positive correlations (red) and negative correlations (blue) with the music playing and autobiographical salience regressors. correlation matrix Acknowledgments: We wish to thank John Ryan, Mike Buonocore, Sonja Rakowski, Susannah Cohen, and Cheryline Mancusi for assistance in collecting the data. Supported in part by NIH R03 DC05146-01. Figure 3. Group activations. Contrast images (beta-estimates) for the regressors of interest (see Fig. 4) from the 14 subject-specific analyses were en- tered into a group analysis. The “music playing” contrast shows regions of activation while music was heard (irrespective of autobiographical salience or emotional valence) relative to periods where responses were being made and the brief inter-trial intervals and rest periods before and after the musi- cal excerpts. The “responses” contrast shows regions of significant activation while response cues were being processed and responses were being made regarding the person’s disposition to the excerpt they just heard. The “autobiographical salience” contrast identifies region of linear activity in- creases across 3 levels of autobiographical salience, and the “positive valence” contrast highlights regions that increased in activity when people found the excerpt they just heard more pleasing. The activations along the medial wall in the autobiographical salience and valence contrasts support the hy- pothesis that regions implicated in self-referential processing would show stronger responses to autobiographically salient pieces of music. L R L R L R Music playing Responses Autobiographical salience Positive valence p<0.001 p<0.001 p<0.001 p<0.005 A D B C Figure 1. Prior studies provide converging evidence for the hypothesis that music, emotion and memories in- teract in the medial prefrontal cortex (MPFC). A) Blood & Zatorre (1999) showed that increasing consonance of melodies with harmonic accompaniment led to increased blood flow in ventral and dorsal MPFC. B) Familiarity judgments about excerpts of real music result in increased MPFC activation (Platel et al., 2003). C) MPFC is rela- tively spared in later stages of Alzheimer’s Disease (AD; Thompson et al., 2003). Patients with advanced AD become cognitively and emotionally engaged with autobiographically salient songs (Cuddy & Duffin, 2005). D) Patterns of activity in MPFC correlate with the pattern of movement of a melody through the tonal space defined by the 24 major and minor keys (represented by the tori on the right; Janata et al., 2002). Figure 2. Characterization of memories and emotions evoked by autobiographically salient pieces of music. A) The top left panel shows the per- centages of stimuli that evoked autobiographical memories across 310 subjects. The other panels show the percentages of the autobiographical stimuli that elicited memories of specific times in one’s life, specific people, or which had an emotional association. Emotional associations are quite common. B) A range of emotions were associated with autobiographically salient songs. C) There was a strong tendency to agree that the specific songs evoked emotional reactions and that the emotions were experienced during that particular presentation of the song. These data indicate that such song excerpts are potent stimuli for inducing a variety of emotions. C B A Conclusions A network of superior temporal, parietal, and lateral (both dorsal and ventral) prefrontal implicated in previous studies of attentive music processing is coactivated with medial prefrontal areas implicated in self-referential processing during the experience of song excerpts that evoke autobiographically salient memories. These results shed light on the interaction of brain networks for interoceptive and exteroceptive processing. Literature Cited Blood, A. J., Zatorre, R. J., Bermudez, P., & Evans, A. C. (1999). Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci, 2(4), 382-387. Cuddy, L. L., & Duffin, J. (2005). Music, memory, and Alzheimer's disease: is music recognition spared in dementia, and how can it be assessed? Medical Hypotheses, 64(2), 229-235. Janata, P., Birk, J. L., Van Horn, J. D., Leman, M., Tillmann, B., & Bharucha, J. J. (2002). The cortical topography of tonal structures underlying Western music. Science, 298(5601), 2167-2170. Platel, H., Baron, J. C., Desgranges, B., Bernard, F., & Eustache, F. (2003). Semantic and episodic memory of music are subserved by distinct neural networks. Neuroimage, 20(1), 244-256. Thompson, P. M., Hayashi, K. M., de Zubicaray, G., Janke, A. L., Rose, S. E., Semple, J., et al. (2003). Dynamics of gray matter loss in Alzheimer's disease. Journal of Neuroscience, 23(3), 994-1005.

Brain networks underlying the retrieval and experience of ...Brain networks underlying the retrieval and experience of music-evoked autobiographical memories. P. Janata* & S.T. Tomic

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Page 1: Brain networks underlying the retrieval and experience of ...Brain networks underlying the retrieval and experience of music-evoked autobiographical memories. P. Janata* & S.T. Tomic

Brain networks underlying the retrieval and experience of music-evoked autobiographical memories. P. Janata* & S.T. Tomic. Center for Mind and Brain, Univ. of California, Davis, Davis, CA. 365.27

IntroductionThe evocation of autobiographical memories and associated emotions by music counts among the most poignant experiences associated with music. Accordingly, excerpts of music can serve as potent retrieval cues with which to study the functional architecture of autobiographical memory. Converging evidence (Figure 1) suggests that the rostral aspect of the medial prefrontal cortex (BA10) is a region where music and autobiographical memories might be integrated. This study tested the hypothesis that experiencing autobiographically salient musical excerpts would result in increased activation in the medial prefrontal cortex.

MethodsPrescreening and memory characterizationAs part of an ongoing survey and description of autobiographical memories evoked by pieces of music, subjects heard 30s excerpts that were selected at random from the Billboard Top 100 Pop and R&B charts from the years in which the subject was between 7 and 19 years of age. Following each excerpt, a subject reported whether the song was familiar and if so whether it evoked a weakly or strongly autobiographical memory or no clear memory at all. For songs identified as autobiographically salient, a more extensive set of questions was administered to probe the specific content of the evoked memory/ies. Subjects were invited to participate in the fMRI version of the experiment if >30% of the excerpts evoked an autobiographical memory.fMRI experiment14 subjects (12 female) were presented with 30 stimuli (selected according to the same criteria as above) across two scanning runs. Excerpts encountered by the subject in the prescreen were excluded from selection. One minute of resting-state activity was recorded prior to the 1st stimulus. Following each excerpt, subjects provided ratings (using left hand) of the affective valence (5-point scale) and arousal (5-pt scale) they experienced while listening to the excerpt, their familiarity with the song (2 pt scale), its autobiographical salience (3 pt scale), and the orientation of their attention toward the memories (5 pt scale) and music (5 pt scale). Immediately following the scanning session, subjects completed a detailed survey about their episodic memories pertaining to songs they correctly identified as having heard in the scanner and flagged as being autobiographically salient. Scanner parameters: Siemens 3T Trio, 34 slices (4 mm thick, 0 skip), TR=2.0s, in-plane resolution: 3.4x3.4 mm. Data were spatially normalized and analyzed in SPM5. See Fig. 4 for examples of subject design matrices.

correlation matrix

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6106

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7031

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+10 +20 +30

+40 +50 +60

05gz

a862

61

-20 -10 +0

+10 +20 +30

+40 +50 +60

-20 -10 +0

+10 +20 +30

+40 +50 +60

-20 -10 +0

+10 +20 +30

+40 +50 +60

-20 -10 +0

+10 +20 +30

+40 +50 +60

-20 -10 +0

+10 +20 +30

+40 +50 +60

Music playing

Individual subject dataDesign Matrices Autobiographical

salience

4

6

8

10

12

-12

-10

-8

-6

-4

t-values (p<0.001)

activ

atio

n

deac

tivat

ion

music playing

autobiographicalsalience

responsesvalence motion

Time

music playing

autobiographicalsalience

responsesvalence motion

Time

0

0.05

0.1

0.15

0.2

0.25

0.3

Strongly Disagree

Disagree

Disagree Som

ewhat

Neither Agree nor D

isagreeAgree Som

ewhat

AgreeStrongly Agree

The song evokesan emotional reaction

0

0.1

0.2

0.3

0.4

Not At All

Very Little

Somew

hat

Fairly Strongly

Very Strongly

The emotion isexperienced ...

aver

age

prop

ortio

n of

auto

biog

raph

ical

stim

uli

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Happy

Calm

ProudC

ontentLovedO

ptimistic

InspiredExcitedInnocentEnergizedStrongJoyousSpiritualR

everentH

opefulBittersw

eetR

ejectedC

hillsYouthfulSadAngryEm

barrassedU

psetD

epressedR

egretfulN

ostalgicC

onfusedJitteryLonelyH

omesick

JealousR

epulsedG

uiltyN

aiveO

ther

Associated emotions

aver

age

prop

ortio

n of

stim

uli

w/a

ssoc

iate

d em

otio

n

0 20 40 60 80 1000

20

40

60

80

#sub

ject

s

% of all stims

Autobiographicalassociation

0 20 40 60 80 1000

20

40

60

80

#sub

ject

s

% of autobiographical stims

Specific timein life

0 20 40 60 80 1000

20

40

60

80

#sub

ject

s

% of autobiographical stims

Specific person

0 20 40 60 80 1000

20

40

60

80

#sub

ject

s

% of autobiographical stims

Emotional association

N=310

Figure 4. Design matrices and activation maps for 3 individual subjects. The 30s presentations of songs are denoted in the design matrices by the white bars in the “music playing” regressors. The set of regressors la-belled “responses” includes both the response cues and responses following each stimulus. The “autobiographi-cal salience” regressor codes a parametric modulation of the stimulus presentation epoch, with an unfamiliar song assuming a value of -1, a weakly autobiographical song a value of 0, and a strongly autobiographical song a value of +1. Valence is coded similarly, with “somewhat” and “strongly” displeasing ratings being coded with -1, neutral ratings with 0, and somewhat and strongly pleasing ratings with +1. Activation maps show regions of significant (p<0.001 unc.) positive correlations (red) and negative correlations (blue) with the music playing and autobiographical salience regressors.

correlationmatrix

Acknowledgments: We wish to thank John Ryan, Mike Buonocore, Sonja Rakowski, Susannah Cohen, and Cheryline Mancusi for assistance in collecting the data. Supported in part by NIH R03 DC05146-01.

Figure 3. Group activations. Contrast images (beta-estimates) for the regressors of interest (see Fig. 4) from the 14 subject-specific analyses were en-tered into a group analysis. The “music playing” contrast shows regions of activation while music was heard (irrespective of autobiographical salience or emotional valence) relative to periods where responses were being made and the brief inter-trial intervals and rest periods before and after the musi-cal excerpts. The “responses” contrast shows regions of significant activation while response cues were being processed and responses were being made regarding the person’s disposition to the excerpt they just heard. The “autobiographical salience” contrast identifies region of linear activity in-creases across 3 levels of autobiographical salience, and the “positive valence” contrast highlights regions that increased in activity when people found the excerpt they just heard more pleasing. The activations along the medial wall in the autobiographical salience and valence contrasts support the hy-pothesis that regions implicated in self-referential processing would show stronger responses to autobiographically salient pieces of music.

L R

L R

L R

Music playing Responses Autobiographicalsalience

Positivevalence

p<0.001 p<0.001 p<0.001 p<0.005

A

D

B C

Figure 1. Prior studies provide converging evidence for the hypothesis that music, emotion and memories in-teract in the medial prefrontal cortex (MPFC). A) Blood & Zatorre (1999) showed that increasing consonance of melodies with harmonic accompaniment led to increased blood flow in ventral and dorsal MPFC. B) Familiarity judgments about excerpts of real music result in increased MPFC activation (Platel et al., 2003). C) MPFC is rela-tively spared in later stages of Alzheimer’s Disease (AD; Thompson et al., 2003). Patients with advanced AD become cognitively and emotionally engaged with autobiographically salient songs (Cuddy & Duffin, 2005). D) Patterns of activity in MPFC correlate with the pattern of movement of a melody through the tonal space defined by the 24 major and minor keys (represented by the tori on the right; Janata et al., 2002).

Figure 2. Characterization of memories and emotions evoked by autobiographically salient pieces of music. A) The top left panel shows the per-centages of stimuli that evoked autobiographical memories across 310 subjects. The other panels show the percentages of the autobiographical stimuli that elicited memories of specific times in one’s life, specific people, or which had an emotional association. Emotional associations are quite common. B) A range of emotions were associated with autobiographically salient songs. C) There was a strong tendency to agree that the specific songs evoked emotional reactions and that the emotions were experienced during that particular presentation of the song. These data indicate that such song excerpts are potent stimuli for inducing a variety of emotions.

CBA

ConclusionsA network of superior temporal, parietal, and lateral (both dorsal and ventral) prefrontal implicated in previous studies of attentive music processing is coactivated with medial prefrontal areas implicated in self-referential processing during the experience of song excerpts that evoke autobiographically salient memories. These results shed light on the interaction of brain networks for interoceptive and exteroceptive processing.

Literature CitedBlood, A. J., Zatorre, R. J., Bermudez, P., & Evans, A. C. (1999). Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci, 2(4), 382-387.Cuddy, L. L., & Duffin, J. (2005). Music, memory, and Alzheimer's disease: is music recognition spared in dementia, and how can it be assessed? Medical Hypotheses, 64(2), 229-235.Janata, P., Birk, J. L., Van Horn, J. D., Leman, M., Tillmann, B., & Bharucha, J. J. (2002). The cortical topography of tonal structures underlying Western music. Science, 298(5601), 2167-2170.Platel, H., Baron, J. C., Desgranges, B., Bernard, F., & Eustache, F. (2003). Semantic and episodic memory of music are subserved by distinct neural networks. Neuroimage, 20(1), 244-256.Thompson, P. M., Hayashi, K. M., de Zubicaray, G., Janke, A. L., Rose, S. E., Semple, J., et al. (2003). Dynamics of gray matter loss in Alzheimer's disease. Journal of Neuroscience, 23(3), 994-1005.