Acta Psychologica 132 (2009) 190–200

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An fMRI investigation on image generation in different sensory modalities: The influence of vividness M. Olivetti Belardinelli a,b,*, M. Palmiero a,b,c, C. Sestieri d,e, D. Nardo a,b, R. Di Matteo b,d, A. Londei b, A. D’Ausilio b, A. Ferretti d,e, C. Del Gratta d,e, G.L. Romani d,e a

Department of Psychology, ‘‘Sapienza” University of Rome, Italy ECONA, Interuniversity Centre for Research on Cognitive Processing in Natural and Artificial Systems, Italy Perceptual and Dynamic Laboratory, Riken Brain Science Institute, Japan d Department of Clinical Sciences and Bio-Imaging, ‘‘G. d’Annunzio” University, Chieti, Italy e ITAB, Institute for Advanced Biomedical Technologies, ‘‘G. d’ Annunzio” University Foundation, Chieti, Italy b c

a r t i c l e

i n f o

Article history: Received 22 July 2008 Received in revised form 14 June 2009 Accepted 22 June 2009 Available online 19 August 2009 PsycINFO classification: 2300 2340 Keywords: Imagery Vividness Sensory-modality Representational format Simulation

a b s t r a c t In the present fMRI study the issue of the specific cortices activation during imagery generation in different sensory modalities is addressed. In particular, we tested whether the vividness variability of imagery was reflected in the BOLD signal within specific sensory cortices. Subjects were asked to generate a mental image for each auditory presented sentence. Each imagery modality was contrasted with an abstract sentence condition. In addition, subjects were asked to fill the Italian version of the Questionnaire Upon Mental Imagery (QMI) prior to each neuroimaging session. In general, greater involvement of sensory specific cortices in high-vivid versus low-vivid subjects was found for visual (occipital), gustatory (anterior insula), kinaesthetic (pre-motor), and tactile and for somatic (post-central parietal) imagery modalities. These results support the hypothesis that vividness is related to image format: high-vivid subjects would create more analogical representations relying on the same specific neural substrates active during perception with respect to low-vivid subjects. Results are also discussed according to the simulation perspective. Ó 2009 Elsevier B.V. All rights reserved.

1. Introduction Mental imagery is considered to be an important component of conscious experience (Paivio, 1969), although it is held to usually occur with a lower intensity when compared to real perception (Fallgatter, Mueller, & Strik, 1997), since it is generated when perceptual information is retrieved from memory, and people are seeing with their ‘‘mind’s eye” (Kosslyn, 1994; Marks, 1973), or hearing with their ‘‘mind’s ear” (Halpern, 1988; Pitt & Crowder, 1992). In recent years, additional experimental evidence demonstrated that people are able to generate mental images also in tactile (Yoo, Freeman, McCarthy, & Jolesz, 2003), kinaesthetic (Jeannerod, 1995), olfactory (Djordjevic, Zatorre, Petrides, & Jones-Gotman, 2004; Elmes, 1998), and gustatory (Kikuchi, Kubota, Nisijima, Washiya, & Kato, 2005) modalities. Although many researchers argue that mental images in different sensory modalities preserve key elements of perceptual stimuli * Corresponding author. Address: Department of Psychology, ‘‘Sapienza” University of Rome, and ECONA, Italy. Tel.: +39 06 49917609; fax: +39 06 4462449. E-mail address: [email protected] (M. Olivetti Belardinelli). 0001-6918/$ - see front matter Ó 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.actpsy.2009.06.009

(Algom & Cain, 1991; Carrasco & Ridout, 1993; Decety & Michel, 1989; Halpern, 1988; Intons-Peterson, 1992; Kosslyn, 1980; Kosslyn, Ball, & Reiser, 1978; Parsons, 1994; Shepard & Metzler, 1971), others state that these representations rely on abstract symbols of the sort used in language (Anderson & Bower, 1973; Pylyshyn, 1973, 1979, 1981, 2002). This debate leads to the issue whether mental imagery and perception share the same mechanisms. The advent of neuroimaging techniques allowed researchers to shed light on the issues of modality-specificity and imagery format (Farah, 2000), addressing at least two different questions: (a) Is there an anatomical separation between the cortical areas serving imagery and those serving perception? (b) Are the areas used for imagery a subset of those engaged in perception? Contrasting results have been provided so far. On one hand, some studies did not report the activation of early sensory areas during imagery tasks (Bunzeck, Wuestenberg, Lutz, Heinze, & Jancke, 2005; D’Esposito et al., 1997; Ishai, Ungerleider, & Haxby, 2000a; Jahn et al., 2004; Mellet, Tzourio, Denis, & Mazoyer, 1998; Mellet et al., 2000). On the other hand, other studies found that perception and imagery share neural networks involving early sensory areas during visual (Amedi, Malach, & Pascual-Leone, 2005;

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Cui, Jeter, Yang, Montague, & Eagleman, 2007; Kosslyn, Thompson, Kim, & Alpert, 1995; Kosslyn et al., 1999), auditory (Bunzeck et al., 2005; Hoshiyama, Gunji, & Kakigi, 2001), tactile (Yoo et al., 2003), olfactory (Bensafi, Sobel, & Khan, 2007; Djordjevic, Zatorre, Petrides, Boyle, & Jones-Gotman, 2005), gustatory (Kikuchi et al., 2005; Kobayashi et al., 2004), and kinaesthetic (Dechent, Merboldt, & Frahm, 2004; Lotze et al., 1999; Porro et al., 1996; Roth et al., 1996; Szameitat, Shen, & Sterr, 2007) imagery. Interestingly, a previous fMRI study from our group (Olivetti Belardinelli et al., 2004a, 2004b) investigated in the same experiment imagery for seven different sensory modalities (visual, auditory, kinaesthetic, olfactory, gustatory, tactile and somatic) triggered by visually presented sentences. Results revealed that all imagery modalities activated mainly two higher associative areas, located in the fusiform gyrus (BA 37) and in the inferior parietal lobule (BA 40), with a slightly different pattern across modalities. Although these divergent results may be partly explained by considering small task differences (e.g., types of images, object categories, stimulus complexity, task requirements and modality of administration; Lambert, Sampaio, Scheiber, & Mauss, 2002), a major confound may be represented by individual differences in the ability to generate mental images. Traditionally, attempts to relate individual differences in imagery abilities were made using self-report questionnaires (Betts, 1909; Galton, 1880). Despite the general methodological criticisms for such methods, questionnaires were developed to test if vividness represents a general imagery ability (Sheehan, 1967) or a modality-specific characteristic (Switras, 1978; White, Ashton, & Law, 1974). Furthermore, specific questionnaires were developed for visual (Marks, 1973), motor (Isaac, Marks, & Russel, 1986), auditory (Gissurarson, 1992) and olfactory (Gilbert, Crouch, & Kemp, 1998) imagery modalities. In recent years neuroimaging techniques addressed the issue of the relationship between subjective and objective measures of imagery. For instance, some studies showed that subjective measures of vividness in visual imagery were associated with BOLD changes in the visual cortex (Amedi et al., 2005; Cui et al., 2007). In the present research, thus, we faced the question whether individual variability in imagery vividness, assessed by means of the Italian version on the Questionnaire Upon Mental Imagery, may be reflected in the activity of the corresponding early sensory cortex for each modality. We predicted that greater involvement of modality-specific cortices should be associated with higher subjective measures of vividness in each sensory modality, representing the specific sensory properties of vivid imagery.

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(e.g., ‘‘the action of writing”); another one related to internal proprioceptive sensations: Somatic (e.g., ”the sensation of fatigue”); and the last one related to Abstract concepts (e.g., racial prejudice). The experimental sentences were in part derived from a previous study (Olivetti Belardinelli et al., 2004a, 2004b) and in part newly constructed on the basis of the same criterion used there (for an English version of the complete list of sentences, see Appendix A). Category distinctiveness of the new sets of experimental sentences was tested. Thirty one subjects (different from those who participated in the fMRI study) filled in a questionnaire and rated the sentences along two dimensions: the dominant imagery modality (multiple choice, including also the ‘‘abstract” option) and the level of vividness (7-point Likert scale). Participants’ responses significantly matched the item classification (p < 0.001), assigning every item to the correct category; moreover modalityspecific items rated as more vivid than abstract items (modalityspecific items: mean 5.15, SD 1.48; abstract items: mean 2.13, SD 1.76; t = 14.74, p = 0.000). The ANOVA on mean vividness scores contrasting category (eight levels – seven imagery modality plus abstract condition) and classification (two levels – matching and no-matching) revealed a main effect for category (F[1,30] = 108,2411, p < 0.001), a main effect for classification (F[7,210] = 21,5074, p < 0.001) and a significant interaction between them (F[7,210] = 5,7524, p < 0.001). The result indicates that coherently classified items were judged more vivid than nonmatching items for all categories except for abstract items; moreover within the coherently classified group only the abstract items differed significantly in vividness scores from all the other categories (Tukey p < 0.001). The selected sentences were first digitally recorded and then post-processed. The gender connotation of the speaker’s voice was concealed using a sound-editing software, in order to reduce the BOLD activation due to the recognition of the speaker’s gender (Imaizumi et al., 2004). A further pre-experimental test, with ten women and ten men, ascertained that each subject attributed the speaker’s voice to a person of her/his own sex. In the fMRI session, the auditory stimuli were delivered through a pneumatic headset, designed to minimize interference from the scanner noise. Sound sampling rate was 22,000 Hz with 16-bit resolution. Stimuli were presented in stereo, at a sound pressure level (SPL) of 85 dB. Despite the high-frequency cut-off of the pneumatic device (estimated around 4 kHz), subjects reported that they were able to clearly hear and understand the meaning of the sentences. 2.3. Procedure

2. Materials and methods 2.1. Subjects Nine, healthy right-handed university students (mean age = 25.2, SD = 3.7) participated in this study. Only female subjects were selected to reduce the gender-related variability that has been reported in imagery tasks (White, Ashton, & Braown, 1977). All of them had normal hearing and vision. Participants gave informed consent for a protocol approved by the local Institutional Ethics Committee and were paid for their participation. 2.2. Stimuli Subjects were stimulated with a set of 96 (12 for each category) auditory short sentences belonging to eight categories: five categories related to different sensory modalities (e.g., Visual: ”to see a candle”; Auditory: ‘‘to hear a shot”; Tactile: ‘‘to touch something hard”; Olfactory: ‘‘the smell of alcohol”; Gustatory: ‘‘the salty taste”); one category related to self-perceived motion: Kinaesthetic

Prior to the scanning session, participants were asked to complete the Italian versions of the Edinburgh Handedness Inventory (Oldfield, 1971) to assess their handedness, and the Questionnaire of Mental Imagery (Sacco & Reda, 1998) to assess their vividness in mental imagery generation in different sensory modalities. The subsequent fMRI session lasted for approximately 40 min, during which both functional and anatomical data were acquired. The paradigm was a classic block paradigm, divided in three runs. Each run consisted of eight blocks (one of imagery in each of the seven sensory modalities plus one abstract block) lasting 28 s and intermixed with rest periods of 20 s. Therefore each run lasted 7 min. During rest periods, subjects were instructed to maintain fixation on a black cross presented at the centre of a white screen. In each block, a cycle of four auditory sentences belonging to one modality at a time was presented. Each cycle consisted of one sentence, lasting 2.5 s, followed by 4.5 s for mental images generation. Subjects were instructed to listen to each sentence, create a mental image of its content and maintain that image until the next sentence was delivered. For the whole fMRI session subjects were explicitly instructed not to move at all, in order to avoid artefacts.

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2.4. Functional imaging Data were acquired with a Siemens Magnetom Vision 1.5 T scanner, by means of T2*-weighted echo planar imaging (EPI) free induction decay (FID) sequences with the following parameters: TR 2698 ms, TE 60 ms, matrix size 64  64, FOV 256 mm, in-plane voxel size 4  4 mm, flip angle 90°, slice thickness 5 mm and no gap. In each run, a total of 155 functional volumes were acquired, consisting of 25 trans-axial slices, including the whole brain. A high-resolution structural volume was acquired at the end of the session via a 3D MPRAGE sequence with the following features: axial, matrix 256  256, FoV 256 mm, slice thickness 1 mm, no gap, in-plane voxel size 1  1 mm, flip angle 12°, TR = 9.7 ms, and TE = 4 ms. 3. Data analysis

nally images were smoothed with a 12 mm full-width-at-halfmaximum (FWHM) isotropic Gaussian kernel to increase the signal-to-noise-ratio and allow a group analysis. 3.2. Statistical analysis on vividness scores Vividness ratings obtained using the Italian version of the Questionnaire of Mental Imagery (QMI) (Sacco & Reda, 1998) were analysed averaging the scores that subjects attributed to respective items for each imagery modality. Therefore, each subject got seven vividness imagery scores, (Table 1-A). In order to split between high and low-vivid subjects a k-means overall analysis was performed on these scores, resulting in two groups with their respective averages in each imagery modality (Table 1-B). Finally, considering the Euclidean distances, a high-vivid group (four subjects) and a low-vivid group (five subjects) were formed (Table 1-C).

3.1. Image preprocessing 3.3. fMRI statistical analysis Data were analysed using MATLAB 7.0 and SPM2 (http:// www.fil.ion.ucl.ac.uk/spm). After discarding the first five images of each session to suppress T1 saturation effects, the 465 whole brain volume images (155 for each session) were realigned and resliced to correct for interscan head movements and then corrected for differences in acquisition time between slices during sequential imaging. The anatomical image of each subject was co-registered to the functional mean image calculated during the realignment. Anatomical images were then spatially normalized to standard brain space (MNI T1 template) using a nonlinear spatial transformation with a 7  8  7 basis function. The estimated nonlinear transformations were then used to reslice the corresponding functional images with a voxel size of 4  4  5 mm. Fi-

Statistical analyses were performed on a voxel-by-voxel basis using the General Linear Model and the theory of Gaussian Random Fields as implemented in SPM2 on the 465 preprocessed images. The design matrix was generated using a block design on a canonical HRF basis function. High pass filtering with a cut-off period of 128 s was carried out and auto-regression was used to correct for serial correlations. The rest condition was modelled implicitly in the design and served as a baseline. At the single-subject level, eight experimental conditions were modelled as explanatory variables (seven imagery modalities – visual, auditory, tactile, gustatory, olfactory, motor, and somatic– plus the abstract concepts) and a voxel-wise t statistic for each condition was

Table 1 (A) Vividness scores obtained on the Vividness Imagery Questionnaire (QMI – Italian Version): low scores indicate high-vividness ratings; high scores indicate low-vividness ratings. (B) Average of each group after K-means analysis, and relative t-test: group 1, low-vividness; group 2, high-vividness. (C) Group members and Euclidean distance from each respective group. A S1 S2 S3 S4 S5 S6 S7 S8 S9

Visual

Auditory

Tactile

Olfactory

Gustatory

Kinaesthetic

Somatic

1.4 1.8 2.4 2.4 1.6 1.6 1.2 2 2.4

3 2 1.4 1.4 1.2 1 2 1.8 2

2 1.6 1.2 2.4 1.6 2.4 1.2 1.4 2

2.2 1.8 1.2 1.6 3 1.8 1.2 2.8 2.2

2 1.4 1.2 1.8 2.2 1.2 1.6 1.4 2.2

2.6 2 1.6 3 2.6 1.4 1.4 2.6 3.4

2 1.6 1.2 2.8 2 2 1.4 2.2 2.4

B Group 1

Group 2

Visual Auditory Tactile Olfactory Gustatory Kinaesthetic Proprioceptive

1.960000 1.880000 1.880000 2.360000 1.920000 2.840000 2.280000

1.750000 1.600000 1.600000 1.500000 1.350000 1.600000 1.550000

t-Test

0.000657145

C High-vivid subjects S2 0.244219

S3 0.35

S6 0.443605

S7 0.345895

Low-vivid subjects S1 0.500057

S4 0.475455

S5 0.430017

S8 0.330886

S9 0.305754

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M. Olivetti Belardinelli et al. / Acta Psychologica 132 (2009) 190–200 Table 2 List of locations of the regions of interest referred to previous related studies. Reference

Anatomical area

BA

Coordinates

Kan et al. (2003) Kosslyn et al. (1999)

Left Fusiform Gyrus Occipital Cortex

Bunzeck et al. (2005)

Heschl Gyrus

37 17 (18/19) (41/42)

Djordjevic et al. (2005) Kikuchi et al. (2005) Yoo et al. (2003) Szameitat et al. (2007)

Piriform–Orbito–Frontal Cortex Anterior Insula Post-Central Gyrus Pre-Central Gyrus

X

11 13 (1/2/3) 4 6

calculated against the rest condition, resulting in a series of statistical parametric maps (SPMs). The contrast images calculated for each voxel at the single-subject level were then entered into the group random-effect analysis. In the group analysis, the different conditions, estimated at the single-subject level, were contrasted as t statistics (random-effect) comparing each imagery modality with the abstract condition. Activated regions were identified as significant only if they reached a height threshold of p < 0.05, corrected (FDR) for multiple comparisons at voxel-level, with a cluster size equal or exceeding 10 contiguous activated voxels (except for post-central activation in the somatic modality in the two-sample t-test analysis). MNI coordinates of the local maxima were then transformed into Talairach coordinates (Talairach & Tournoux, 1988) using the MNI2Tal provided by M. Brett (http://www.mrc-cbu.cam.ac.uk/imaging/common/mnispace.shtml) and activated areas were labelled according to the Talairach Daemon Database (http://ric.uthscsa.e-

Y 45 2 34 44 40 27 44 57 18 32

Z 53 88 86 10 20 6 10 27 30 7

6 12 12 8 8 11 2 38 60 50

du/resources/body.html). In addition, a small volume correction (SVC) was performed on both hemispheres using a 10 mm radius within anatomical regions of interest (ROIs). The locations of the regions of interest were based on a priori hypotheses drawn from previous related studies (see Table 2).

4. Results 4.1. Relevant activation for the whole sample The one sample t-test analysis comparing each imagery modality versus the abstract condition was performed to explore what process imagery modalities have in common once critical components involved both in imagery and in the abstract condition are subtracted (e.g., task initiation and maintenance, attention, and working memory). In general, the activation of the left fusiform

Table 3 Stereotaxic coordinates (Talairach & Tournoux, 1988), anatomical locations, and T scores of (local) peak activations for the comparison Imagery Modality > Abstract. The X sign indicates Small Volume Correction applying. Imagery modality

Antomical area

BA

Coordinates X

Cluster Y

Z

SVC

p (cor)

K

T

Visual

L Fusform Gyrus L Fusform Gyrus

37 37

48 40

64 58

13 6

0.035

113

4.74 5.01

Auditory

L Fusiform Gyrus L Middle Temporal Gyrus L Caudate Tail

37 37

45 55 36

58 58 35

7 1 2

0.049

14

3.52 3.52 4.54

Tactile

L Superior Temporal Gyrus L Fusform Gyrus L Caudate Tail

22 37

44 40 36

27 47 39

2 8 2

0.032 0.032

14 14

2.60 5.27 2.70

L L L L L L

7 7 7 30 37

16 20 16 16 48 32

71 64 60 39 64 42

50 40 49 7 11 7

0.609

85

0.039 0.039

16 16

4.43 2.93 2.89 3.44 5.04 3.41

Olfactory

Precuneus Precuneus Precuneus Parahippocampal Gyrus Fusform Gyrus Hippocampus

Gustatory

L Fusform Gyrus L Caudate Tail

37

51 36

59 27

10 3

0.049

10

4.38 5.25

Kinaesthetic

L L L L L L L L

2 5 6 6 20 37 40

24 36 20 16 32 24 44 24

36 44 17 13 36 40 40 56

66 62 56 47 15 15 57 31

0.339

64

0.009

43

0.027 0.042 0.339 0.042

22 15 64 15

4.09 4.12 9.31 5.07 3.82 3.46 4.42 5.02

19 19 36 37 37

40 40 28 51 40

75 79 32 63 47

13 17 15 14 14

0.000 0.001 0.000 0.001 0.000

89 53 89 53 89

9.40 7.00 5.79 9.09 7.56

Somatic

Post-Central Gyrus Paracentral Gyrus Middle Frontal Gyrus Medial Frontal Gyrus Fusform Gyrus Fusform Gyrus Inferior Parietal Lobule Cerebellum

R Fusiform Gyrus L Fusform Gyrus R Limbic Parahippocampal Gyrus L Fusform Gyrus R Fusiform Gyrus

X

X X

X X X

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gyrus (BA37) was found for all the imagery modalities. The somatic imagery yielded also the activation of the right fusiform gyrus (BA37) and of the bilateral occipital fusiform gyrus (BA19), whereas, the kinaesthetic imagery resulted in the activation of the left fusiform gyrus (BA20). Activations are listed in Table 3 and shown in Fig. 1. 4.2. Modality-specific activation The two-sample t-test analysis comparing high-vivid versus low-vivid subjects, within each imagery modality contrasted with the abstract condition, showed significantly greater activations in sensory specific areas for high-vivid compared to low-vivid subjects. Specifically, we observed greater activity for the high-vivid

subjects in: the left inferior occipital gyrus (BA17/18) for visual imagery; the left anterior insula (BA13) for gustatory imagery; the right post-central gyrus (BA2) for tactile and somatic imagery; and the left pre-central gyrus (BA4) for kinaesthetic imagery. Activations are listed in Table 4 and presented in Fig. 2. In order to clarify the differences between the activation patterns of high- and low-vivid subjects, a ROI analysis (implemented as SVC) was performed in relevant sensory specific areas. As shown in Fig. 3, activity in these areas was enhanced in high-vivid subjects and deactivated in low-vivid subjects. This was observed for all sensory modalities we tested. In general, the analysis showed significant activities in each ROI only during the associated sensory modality (i.e. visual cortex ROI showed activity during visual imagery only).

Fig. 1. Activation of the left Fusiform gyrus for the comparison Imagery Modality > Abstract.

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Table 4 Stereotaxic coordinates (Talairach & Tournoux, 1988), anatomical locations, and T scores of (local) peak activations for the comparison Imagery Modality > Abstract in high-vivid with respect to low-vivid subjects. The X sign indicates Small Volume Correction applying. Imagery modality

Antomical area

BA

Coordinates X

Cluster Y

Z

p (cor)

SVC K

T

Visual

L Inferior Occipital Gyrus L Inferior Occipital Gyrus

17 18

16 32

90 82

8 4

0.029 0.021

21 27

4.53 5.52

X X

Auditory

L Middle Frontal Gyrus L Middle Frontal Gyrus L Middle Frontal Gyrus R Transverse Temporal Gyrus L Transverse Temporal Gyrus

10 10 10 42 42

44 28 36 67 56

47 63 59 19 16

11 11 11 10 14

0.940

90

0.194 0.145

23 47

4.83 3.76 3.62 5.80 4.86

X X

Tactile

R Post-Central Gysrus R Superior Frontal Gyrus R Inferior Parietal Lobue L Cerebellum (Anterior Lobe)

2 10 40

55 28 48 16

25 47 40 44

52 16 53 23

0.038 0.901 0.909 0.367

20 33 32 86

4.34 5.78 4.34 5.89

X

Olfactory

R Middle Frontal Gyrus L Middle Frontal Gyrus L Middle Frontal Gyrus R Insula L Fusiform Gyrus R Inferior Parietal Lobule

6 10 10 13 37 40

48 32 32 40 48 48

14 50 40 11 64 40

45 7 16 6 11 53

0.035 0.288 0.288 0.075 0.039 0.975

19 536 26 7 16 148

5.07 5.48 3.60 3.10 5.47 4.34

X

L L L L

Middle Frontal Gyrus Anterior Insula Superior Temporal Gyrus Transverse Temporal Gyrus

10 13 38 42

44 36 32 56

47 16 3 16

11 5 13 14

0.948 0.021 0.936 0.145

90 28 95 47

4.83 3.82 2.95 4.86

L Post-Central Gyrus L Pre-Central Gyrus L Cerebellum (Anterior Lobe) R Cerebellum (Anterior Lobe)

3 4

32 32 12 16

25 21 41 44

43 52 32 27

0.017 0.017 0.000 0.000

14 14 236 236

6.39 6.39 9.30 12.34

R Post-Central Gyrus R Superior Parietal Lobule R Superior Parietal Lobule

2 7 7

51 40 28

28 67 60

57 49 50

0.047

3

3.54 3.86 3.04

Gustatory

Kinaesthetic

Somatic

X X

X X X

X

Fig. 2. Activation of sensory specific cortices for each imagery modality contrasted with abstract condition in high-vivid subjects with respect to low-vivid subjects.

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Fig. 3. Histograms of contrast estimates and 90% Confidential Interval for each ROI contrasting high- versus low-vividness for each imagery modality. For visual, auditory modalities, the contrasts are shown in two different areas: left BA 17 and left BA 18 for visual imagery.

4.3. Correlation analysis A regression analysis was also performed to regress the BOLD signals onto the vividness scores and to better predict the activations in modality-specific areas. This analysis was done considering the contrasts at single-subject level between imagery modality and abstract condition. In general, specific-modality cortices were found positively correlated with vividness scores for visual, tactile, gustatory, kinaesthetic and somatic imageries. In particular, activations of the right lingual and inferior occipital gyrus (BA18), as well as of the bilateral middle occipital gyrus (BA19) were found for the visual imagery modality. In addition, the right post-central gyrus (BA2) for tactile imagery, the left anterior insula (BA13) for gustatory imagery, the left pre-central gyrus (BA6) for kinaesthetic imagery, and the right post-central gyrus (BA3) for somatic imagery were found activated significantly. For the complete list of activations, refer Table 5. 5. Discussion In the last decade, neuroimaging studies offered critical insights into the long standing mental imagery debate. In fact, the neural bases of mental image generation have been investigated in all the sensory modalities, showing that both modality-specific and a-specific areas are involved. Nevertheless, few studies focused on the differences or similarities for all imagery modalities and

on the possible influence of vividness variability on cortical activity. In this study we tested whether the fMRI BOLD signal was modulated in sensory cortices according to the individual variability in vividness in all imagery modalities, using a set of sentences similar to the one originally used by Olivetti Belardinelli et al. (2004a, 2004b). 5.1. Relevant activations to all subjects (high- and low-vivid) We compared each imagery modality with the abstract condition in the whole sample in order to better investigate the processes underlying the imagery operations, excluding attentional, conceptual and working memory processes. The left fusiform gyrus (BA37) was found active for all imagery modalities. In general, this area has been related to semantic retrieval during a property verification task when associated false trials were present and in absence of explicit mental imagery instructions (Kan, Barsalou, Solomon, Minor, & Thompson-Schill, 2003). Moreover, it has been related to visual mental imagery (D’Esposito et al., 1997), object recognition (Ishai, Ungerleider, Martin, & Haxby, 2000b), and retrieval of object information (Price, Noppeney, & Phillips, 2003). Nevertheless, since we used verbal cues to elicit images, the left fusiform activation may also reflect a visual semantic retrieval (Thompson-Schill, Aguirre, D’Esposito, & Farah, 1999), which gives rise to multi-modal mental representation (e.g., visuo-olfactory, visuo-gustatory, etc., as shown in Olivetti Belardinelli et al., 2004a),

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Table 5 Stereotaxic coordinates (Talairach & Tournoux, 1988), anatomical locations, and T scores of (local) peak activations for the comparison Imagery Modality > Abstract regressed onto the vividness ratings. The X sign indicates Small Volume Correction applying. Imagery modality

Antomical area

BA

Coordinates X

Visual

Cluster Y

Z

p (cor)

SVC K

T

R Middle Frontal Gyrus R Middle Frontal Gyrus L Middle Frontal Gyrus R Superior Frontal Gyrus L Superior Fronta Gyrus R Superior Frontal Gyrus R Lingual Occipital Gyrus R Inferior Occipital Gyrus R Middle Occipital Gyrus L Middle Occipital Gyrus L Posterior Cingulate R Posterior Cingualte R Cingualte Gyrus R Anterior Cingualte R Sovramarginal Gyrus L Inferior Parietal Lobule

6 6 6 9 10 10 18 18 19 19 24 30 31 32 40 40

40 44 28 16 24 24 16 36 48 24 4 8 16 8 40 40

6 14 2 52 44 48 82 86 74 82 34 50 53 43 41 45

46 45 42 20 16 21 9 4 6 17 20 16 26 12 30 38

0.042 0.001 0.000 0.032 0.000 0.032 0.000 0.042 0.000 0.007 0.000

52 107 125 55 125 55 401 52 401 19 126

0.032 0.000

55 401

R Middle Frontal Gyrus R Insula L Lingual Gyrus R Posterior Cingulate R Angular Gyrus R Superior Temporal Gyrus L I nferior Frontal Gyrus R Inferior Frontal Gyrus

10 13 19 23 39 42 44 47

36 40 28 4 45 67 51 51

51 16 74 30 68 19 1 39

3 13 1 20 31 10 18 2

0.77

102

0.000 0.000 0.000 0.078 0.131 0.085

1438 1438 1438 35 18 32

5.05 3.02 10.06 5.7 11.3 2 4.35 2.34

Tactile

R Post-Central Gyrus R Anterior Insula R Post-Central Gyrus L Lingual Gyrus R Superior Temporal Gyrus L Post-Central Gyrus R Cerebellum (Anterior Lobe)

2 13 5 18 38 43

48 36 32 12 51 51 28

28 26 44 82 19 18 52

52 15 57 9 14 19 27

0.005 0.001 0.005 0.000 0.001 0.000 0.035

27 146 27 669 146 387 74

7.4 4.02 5.99 6.65 7.02 12.3 4.35

Olfactory

R Middle Frontal Gyrus R Middle Frontal Gyrus R Middle Frontal Gyrus

10 10 10

45 28 40

50 55 52

11 20 20

0.996

93

3.43 3.38 3.37

Gustatory

L Anterior Insula L Anterior Insula L Post-Central Gyrus

13 13 43

40 36 59

1 7 6

14 14 19

0.05 0.05 0.05

16 16 16

4.27 4.21 4.4

Kinaesthetic

R Medial Frontal Gyrus R Medial Frontal Gyrus L Pre-Central Gyrus L Middle Frontal Gyrus R Cuneo L Inferior Parietal Lobule L Inferior Parietal Lobule

6 6 6 6 18 40 40

4 12 32 40 24 55 59

17 20 6 2 84 29 30

52 56 33 41 23 38 29

0.049

22

0.05

12

0.95

90

6.45 5.8 4.57 3.1 3.35 4.19 3.78

R Post-Central Gyrus L Medial Frontal Gyrus R Medial Frontal Gyrus L Superior Temporal Gyrus L Inferior Frontal Gyrus

3 6 6 22 44

24 4 12 63 59

28 9 24 50 16

57 47 56 12 13

0.002

545

0.004

494

Auditory

Somatic

as well as cross-modal interaction (Olivetti Belardinelli et al., 2004c). 5.2. Modality-specific activations When the abstract condition was subtracted from the imagery generation process, activation of sensory specific cortices appears to be modulated by vividness scores and critically more significant activity was found in high-vivid subjects only with respect to lowvivid, except for auditory and olfactory imagery. Regarding auditory imagery, the lack of significant modality-specific activation may be due to the interference of the scanner noise on the auditory image formation process. In fact, contrasting an experimental and baseline condition with continuous scanner background noise, Gaab, Gabrieli, and Glover (2007) demonstrated that both may lead

4.03 7.13 6.06 4.92 4.9 4.77 6.95 7.5 4.74 5.05 9.27 4.27 4.36 4.89 8.36 8.28

X

X

X X X

6.5 7.56 7.21 5.25 5.25

to signal decreases, with a greater effect in Heschl’s gyrus. Regarding olfactory imagery, the lack of an olfactory activation leads to the conclusion that the vividness scores related to olfactory imagery do not predict olfactory specific-modality activations, probably depending on the difficulty in generating vivid images of smells (Lawless, 1997), especially when they are verbally cued (Herz, 2000). With respect to conditions revealing significant activity, although correlation and group analyses do not completely overlap, both analyses revealed that modality-specific activations are modulated by vividness level for visual, tactile, gustatory, kinaesthetic and somatic mental imageries. In particular, for visual imagery, the activation of BA17 (group analysis) or BA18 (both group and correlation analysis) was found. Several studies provided no evidence of these activations – for

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instance, when participants generated images of objects, faces or animals starting from concrete nouns or sentences (D’Esposito et al., 1997; Ishai et al., 2000a; Mellet et al., 1998; Olivetti Belardinelli et al., 2004a, 2004b), as well as when individuals were required to generate and inspect letters (Goldenberg et al., 1989; Gulyas, 2001), or previously memorized maps (Ghaem et al., 1997; Mellet, Tzourio, Denis, & Mazoyer, 1995; Mellet et al., 2000). Nevertheless, early visual cortex activation was found in many other studies (Goldenberg et al., 1989; Goldenberg, Steiner, Podreka, & Deecke, 1992; Kosslyn et al., 1993, 1995, 1999). Consistent with the present data, a recent study reported that visual cortex activity was correlated with reported vividness, demonstrating that individual differences in mental imagery vividness are detectable by means of fMRI (Amedi et al., 2005; Cui et al., 2007). For tactile imagery, the right post-central gyrus (BA2) was found activated in high-vivid subjects as compared to low-vivid ones, as well as correlated with the vividness ratings. This lateralization is probably not due to the handedness of the subjects, since we recruited only right-handed subjects, nor to a tactile tentative exploration by hand, since we asked subjects to avoid any type of movement during the scanning session, but more likely to the subjective component of tactile sensation (Querleux et al., 1999). In fact, even though Yoo et al. (2003) demonstrated an activation of the left post-central gyrus (BA 1/2/3) when subjects imagined a tactile stimulation on the back of the right hand (specifically when comparing tactile imagery with resting conditions), Querleux et al. (1999) found an activation mostly localized in the ipsilateral somato-sensory cortex during the imagination period of tactile stimulation and a more strong activation of the contra-lateral cortex during the period of tactile perception. Regarding gustatory imagery, the left anterior insula (BA13) was found active in both the analyses that were carried out, as well as the left middle frontal gyrus when high-vivid subjects were compared to low-vivid ones. These results contrast with those of Kikuchi et al. (2005) and with those of Olivetti Belardinelli et al. (2004b), which revealed activations in the right insula during image generation of tastes, but they are in accordance with those of Kobayashi et al. (2004), who found activations in the left and bilateral insulae during gustatory imagery and perception, respectively, and in the middle and/or superior frontal gyri. According to these authors, the left insula also processes higher gustatory information by receiving a signal from the regions in the frontal cortex that may mediate the ‘‘top-down” control of retrieving gustatory information from long-term memories. Concerning kinaesthetic imagery, the pre-central gyrus (BA4) and the anterior cerebellum were found activated in high-vivid subjects only, as well as the pre-central gyrus (BA6) with a correlation analysis. Once more, for motor imagery too, the literature provides contrasting results. Jahn et al. (2004) did not report any activation of motor cortices during the imagery of everyday complex movements. However, the motor cortices, although with different patterns of activation, were found active during the mental representation of movements with the left or the right hand (Dechent et al., 2004; Lotze et al., 1999; Porro et al., 1996; Roth et al., 1996) and complex everyday movements like eating a meal, or swimming (Szameitat et al., 2007). The anterior cerebellar activation is consistent with the view of a temporal processing of sensory and motor information (Ivry, 1996), suggesting that the cerebellum is able to extract kinematic information relative not only to the movement itself (Kavounoudias et al., 2008), but also to kinaesthetic imagery as well. Considering the debate as to whether the primary motor area may be recruited during kinaesthetic imagery, and the evidence that the Post-central Gyrus (BA 3) was found active as well as the BA 4, this activation revealed in the present study must be interpreted with caution.

Finally, the somatic imagery modality has shown, in high-vivid as compared with low-vivid subjects, the recruitment of the right post-central gyrus (BA2) with a cluster size of three voxels only and a correlation with the right post-central gyrus (BA3). Although no other study has been carried out on this modality except those of Olivetti Belardinelli et al. (2004a, 2004b), besides in agreement with the results in the present study, the somato-sensory activation (post-central gyrus) yielded by the somatic imagery system is in line with studies involving vibro-tactile stimulation (Leblanc, Mayer, Zatorre, Tampieri, & Evans, 1995).

5.3. Modality-specific deactivations The analysis comparing the low-vivid subjects with the high-vivid ones did not show any significant activation in modality-specific areas. As shown by the histograms of effect sizes (Fig. 3), the low-vivid subjects even reported deactivations in the same areas that are vice versa activated by the high-vivid subjects. Deactivations are normally observed in a rival cortical area during mental imagery (Amedi et al., 2005). Nevertheless, Buckner, Raichle, Miezin, and Peterson (1996) found that occipital deactivations can occur when people generate visual images from verbal cues in order to recall previously learned objects. According to the authors, these deactivations reflect a cross-modal inhibition process, given the auditory-directed attention paid to the words. Interestingly, Mellet et al. (2000) found a significant decrease of rCBF in the primary visual area when subjects were asked to perform on a high-resolution imagery task recollecting material visually, rather than verbally. Although in this case the authors explicitly claim that it is hard to account for such a result, they attempt to explain this puzzling deactivation referring to it as a top-down modulation. In the present study, since imagery was triggered by auditory sentences, it is possible to interpret the deactivations in our low-vivid subjects as caused by a crossmodal inhibitory mechanism involving a verbal attention processing. Anyway, this pattern of results challenges the hypothesis whether low-vivid subjects use a completely different network with respect to the high-vivid ones. Therefore, the distinction between simulation account of conceptual knowledge processing and mental imagery has to be taken into consideration. As pointed out extensively by Barsalou (1999, 2008a, 2008b) and Barsalou, Santos, Simmons, and Wilson (2008), simulation representing conceptual knowledge occurs as re-enactment of perceptual, motor, and introspective states acquired during a particular experience. Mental imagery is a conscious simulation in working memory, whereas, other forms of simulation are unconsciously outside working memory (Barsalou, 1999, 2008a). Since in the present experiment subjects were explicitly instructed to perform a mental imagery process, the simulation account fits well with the results obtained from our high-vivid subjects. This is not the case for our low-vivid subjects’ results, which did not show any modality-specific activation. More likely, given the deactivation patterns, the low-vivid subjects produced conscious semantic representations based on available linguistic information, rather than unconscious simulations partially reactivating perceptual experiences. Therefore, it is possible that low-vivid subjects are more confident in a conscious verbal-semantic strategy to achieve imagery generation and use their knowledge of physical principles in the real world to simulate how things would appear under actual physical conditions corresponding to the tasks (Pylyshyn, 2002). Although this interpretation may be consistent with the propositional view, further studies are necessary to better address this issue, as well as the nature of deactivations.

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Appendix A (continued)

6. Conclusions According to our hypothesis, the level of imagery vividness in different sensory modalities may be related to differences of BOLD activity in modality-specific cortices. In other words, some of the neural processes underlying modality-specific perception may also be used in imagery when people are able to evoke vivid images. In particular we found modality-specific activation for visual, tactile, gustatory, kinaesthetic and somatic imagery modalities when subjects generated and maintained mental images triggered by auditory sentences. These results are consistent with the view that the ability of generating vivid images may have an influence on the process of image formation on both the format and the activation levels, high-vivid subjects creating more analogical images and sharing very similar neural mechanisms with perception as compared to low-vivid subjects. In the future, in order to better specify this difference we are planning to compare the fMRI results of high- and low-vivid subjects with their ratings, after the fMRI session, of the perceived vividness of the image generated by each stimuli sentence.

Appendix A Visual sentences

Auditory sentences

Tactile sentences

Gustatory sentences

To see a bulb

To hear a whistle To hear a rumble To hear a tinkling To hear a snap

To touch something grainy To touch something velvety To touch something sharp To touch something sticky To touch something liquid To touch something hard To touch something smooth To touch something gelatinous To touch something soft To touch something rough To touch something gummy To touch something greasy

The salty taste

To see a bucket To see a coin To see a cloud To see a book

To hear grating

To see a glass

To hear a shot

To see a box

To hear ringing

To see a hat

To hear thunder To hear a chime To hear buzzing To hear a rustle To hear an uproar

To see a candle To see a pencil To see a house To see a tree

The sweet taste The sour taste The rancid taste The sweet and sour taste The spicy taste The acidic taste The tart taste The bitter taste The fruity taste The peppery taste The unripe taste

Olfactory sentences

Kinaesthetic sentences

Somatic sentences

Abstract sentences

The stale smell The smell of sewage The burning smell The smell of alcohol The smell of gas The smell of paint The smell of leather

The action writing The action jumping The action painting The action walking The action kicking The action pulling The action lifting

The sensation shivers The sensation excitement The sensation irritation The sensation pain The sensation fatigue The sensation creeps The sensation exertion

of

The legal technicality The power of reason Syntactical correctness The spiritual power The cardinal sin

of the

Racial prejudice

of

Innate goodness

of of of of of of of

of of of of

Olfactory sentences

Kinaesthetic sentences

Somatic sentences

Abstract sentences

The smell of lavender The clean smell

The action of pushing The action of throwing The action of running The action of swimming The action of dancing

The sensation of cramps The sensation of cold

Formal logic

The smell of bread The fried smell The moldy smell

The sensation of nausea The sensation of drunkenness The sensation of freshness

The lack of honesty Universal domination Classical physics Judging on intention

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