Cogn Process (2009) 10 (Suppl 2):S268–S271 DOI 10.1007/s10339-009-0324-5

EXTENDED ABSTRACT

Mental imagery generation in different modalities activates sensory-motor areas Massimiliano Palmiero Æ Marta Olivetti Belardinelli Æ Davide Nardo Æ Carlo Sestieri Æ Rosalia Di Matteo Æ Alessandro D’Ausilio Æ Gian Luca Romani


Marta Olivetti Belardinelli and Springer-Verlag 2009

Introduction Psychological science paid great attention to the embodied cognition perspective, focusing on interaction between thought and action, as well as between rational and sensorymotor schemas (Lakoff and Johnson 1999). From this perspective, cognition relies on experiences allowed by a body, which interacts with the environment by means of particular perceptual and motor capacities. These capacities form the frame within which all cognitive processes are meshed (Thelen et al. 2001). Indeed, conceptual knowledge about objects activates the visual areas (Martin 2007). Similarly, when people process foods conceptually, gustatory areas are recruited (Simmons et al. 2005), whereas when they read sentences regarding smells, olfactory areas become active (Gonzalez et al. 2006). Both retrieval and comparison of semantic features of running, hitting, and cutting verbs M. Palmiero (&)
M. Olivetti Belardinelli
D. Nardo Department of Psychology, ‘‘Sapienza’’ University of Rome, Rome, Italy e-mail: [email protected] M. Palmiero
M. Olivetti Belardinelli
D. Nardo
R. Di Matteo
A. D’Ausilio ECONA, Interuniversity Centre for Research on Cognitive Processing in Natural and Artificial Systems, Rome, Italy M. Palmiero Perceptual and Dynamic Laboratory, Riken Brain Science Institute, Wakoshi, Japan C. Sestieri
R. Di Matteo
G. L. Romani Department of Clinical Sciences and Bio-Imaging, ‘‘G. d’Annunzio’’ University, Chieti, Italy C. Sestieri
G. L. Romani ITAB, Institute for Advanced Biomedical Technologies, ‘‘G. d’ Annunzio’’ University Foundation, Chieti, Italy

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involve primary motor and pre-motor cortices (Kemmerer et al. 2008). Finally the neuroscientific approach confirmed that cognition is grounded in sensory-motor brain systems as simulations (Barsalou 2008). Nevertheless, different types of simulations are possible, such as mental imagery, which is considered a conscious representation in working memory (Barsalou 2008). Neuro-imaging studies provided strong evidences of modal activations for visual (Klein et al. 2004), auditory (Hoshiyama et al. 2001), tactile (Yoo et al. 2003), olfactory (Djordjevic et al. 2005), gustatory (Kikuchi et al. 2005), and motor (Szameitat et al. 2007) imagery modalities. The aim of this study is therefore to investigate whether imagery in different sensory modalities triggered by verbal stimuli relies on the embodied perspective, and thus whether imagery implies sensory-motor activations. Moreover, considering the Gibbs and Bergs’ challenge (2002), according to which imagery depends on action, we face the issue to verify whether mental imagery in different modalities involves the activation of motor cortices (e.g., pre-motor areas).

Method The study focused on imagery related to seven sensory modalities (derived from the five senses and from motor actions and proprioception), which were compared to the mental representation of abstract concepts. In total 96 auditory short sentences (12 for each imagery modality plus 12 for abstract condition: see Olivetti Belardinelli et al. 2009) were auditory presented to nine healthy righthanded female subjects (mean age = 25.2, SD = 3.7). Prior to the scanning session, subjects’ handedness and vividness in mental imagery generation in different sensory modalities were assessed by means of the Edinburgh

Cogn Process (2009) 10 (Suppl 2):S268–S271

Handedness Inventory, (Oldfield 1971) and of the Questionnaire of Mental Imagery (QMI: Sacco, Reda 1998) respectively. As regards the fMRI sessions, a block paradigm was used, divided in three randomly assembled runs. Each runs consisted of eight task blocks (seven for imagery modalities plus one for abstract condition) of 28 s., intermixed with rest period of 20 s. In each task block, a cycle of four auditory sentences belonging to one imagery modality was presented (each sentence lasting for 2.5 s and followed by 4.5 s of relative mental images generation). Subjects were instructed to create a mental image of the content of each sentence and maintain the image until the next sentence was delivered.

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contrasted with the abstract condition was performed. Results showed significant activations in modality-specific cortices for visual, tactile, gustatory, kinaesthetic and somatic imagery modalities. Although without a complete overlapping, modality-specific activations were confirmed regressing the BOLD signals onto the vividness scores, as measured with the QMI. Finally, all contrasts comparing each imagery modality versus rest showed activity in the precentral gyri (BA6), in the left or right hemisphere according to the modality considered (coordinates for each significant activation are carefully reported in Table 1 according the kind of analysis performed).

Discussion Vividness scores analysis In order to distinguish between high- and low-vivid subjects a k-means overall analysis on QMI vividness ratings was performed, obtaining a distinction between a high-vivid group (four subjects) and a low-vivid group (five subjects). fMRI analyses Data were acquired with a Siemens Magnetom Vision 1.5 T scanner. Statistical analyses were performed on a voxelby-voxel basis using the General Linear Model and the theory of Gaussian Random Fields as implemented in SPM2. All volumes were realigned, slice timed co-registered and normalized; finally a spatial Gaussian filter 12 mm FWHM was applied. The design matrix was generated using a block design on a canonical HRF basis function. The rest condition was modelled implicitly in the design and served as baseline. In the group analysis, the different conditions were contrasted as t statistics (random-effect) comparing each imagery modality with the abstract or rest condition. Regions activated were identified as significant for P \ 0.05 (corrected for multiple comparison FDR), with a cluster size equal or exceeding ten contiguous activated voxels. MNI coordinates of the local maxima were then transformed into Talairach coordinates (Talairach and Tournoux 1988) using the MNI2Tal provided by M. Brett and activated areas were labelled using the Talairach Daemon Database. Within anatomical regions of interest (ROIs) a small volume correction (SVC) was applied (10 mm radius). The locations of ROIs were based on a priori hypotheses.

Results To compare high-vivid versus low-vivid subjects a two sample t test analysis within each imagery modality

For the most of the imagery modalities investigated the vividness level of images generated significantly correlated with activations in the corresponding modality-specific systems (except for the auditory and the olfactory ones). Regarding auditory imagery on the contrary, 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 et al. (2007) demonstrated that both may lead to signal decreases, with a greater effect in Heschl’s gyrus. As regarding the 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, especially when they are verbally cued (Herz 2000). More interestingly, we also found the recruitment of the pre-motor cortex. apart from the vividness level. Research demonstrates that activation of pre-motor cortex is important for the representation of action in abstract terms of its purpose (Garbarini, Adenzato 2004). Therefore, considering our results, a key role of pre-motor cortex is suggested in the re-enactment of sensory-motor systems also for nonkinesthetic imagery generation process. In other words, imagery can involve the recruitment of a multi-modal network, reflecting a concept-driven motor involvement when mental images in different sensory modalities are generated in response to spoken sentences. According to this pattern of activity, mental imagery appear to be fundamentally grounded in people’s sensorymotor systems, involving also a degree of conscious experience which embodied activity in the real world. In this view, mental imagery provides the building blocks for cognition (e.g., thinking, memory, etc…) (Gibbs and Bergs 2002), and involves intentional mental states of action episodes that are created in response to external stimuli.

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Table 1 Stereotaxic coordinates (Talairach and Tournoux 1988), anatomical locations and level of significance for the comparisons imagery modality [ abstract in two sample t test, regression and one sample t test analyses. The X sign indicates small volume correction applying Imagery modality

Anatomical area

BA

Coordinates X

Cluster

Y

Z

p (cor)

SVC K

T

Two sample t test analysis: imagery modality versus abstract condition Visual

L inferior occipital gyrus

17

–16

-90

-8

0.029

21

4.53

X

Tactile

L inferior occipital gyrus R postcentral gyrus

18 2

-32 55

-82 -25

-4 52

0.021 0.038

27 20

5.52 4.34

X X

Gustatory

L anterior insula

13

-36

16

5

0.021

28

3.82

X

Kinaesthetic Somatic

L postcentral gyrus

3

-32

-25

43

0.017

14

6.39

X

L precentral gyrus

4

-32

-21

52

0.017

14

6.39

X

R postcentral gyrus

2

51

-28

57

0.047

3

3.54

X

R superior parietal lobule

7

40

-67

49

3.86

R superior parietal lobule

7

28

-60

50

3.04

Regression analysis: imagery modality versus abstract condition Visual

R lingual occipital gyrus

18

16

-82

-9

0.000

401

6.95

R inferior occipital gyrus

18

36

-86

-4

0.042

52

7.5

R middle occipital gyrus

19

48

-74

6

0.000

401

4.74

L middle occipital gyrus

19

-24

-82

17

0.007

19

5.05

X

2

48

-28

52

0.005

27

7.4

X

Tactile

R postcentral gyrus

5

32

-44

57

0.005

27

5.99

Gustatory

L anterior insula L anterior insula

13 13

-40 -36

1 -7

14 14

0.05 0.05

16 16

4.27 4.21

L postcentral gyrus

43

-59

-6

19

0.05

16

4.4

X

6

4

-17

52

0.049

22

6.45

X

0.05

12

R postcentral gyrus

Kinaesthetic

Somatic

R medial frontal gyrus R medial frontal gyrus

6

12

-20

56

L precentral gyrus

6

-32

-6

33

5.8

L middle frontal gyrus

6

-40

2

41

R postcentral gyrus

3

24

-28

57

L medial frontal gyrus

6

-4

-9

47

7.56

R medial frontal gyrus

6

12

-24

56

7.21

4.57

X

3.1 0.002

545

6.5

One sample t test analysis: imagery modality versus rest condition Visual Auditory

L precentral gyrus

6

-12

3

55

L precentral gyrus

6

-20

-14

61

R precentral gyrus

6

28

-6

55

R precentral gyrus

6

40

-9

51

0.013

122

7.62 4.43

0.044

92

6.78 5.20

Tactile

L precentral gyrus

6

-32

-13

54

0.000

783

8.94

Olfactory

L precentral gyrus L middle frontal gyrus

6 6

-36 -32

-5 3

65 60

0.028

11

5.21 5.40

X

Gustatory

R precentral gyrus

6

63

-2

32

0.021

28

3.82

X

Kinaesthetic

L precentral gyrus

6

-24

-15

61

0.000

104

9.70

L middle frontal gyrus

6

-48

14

45

0.002

193

L precentral gyrus

6

-40

7

55

Proprioceptive

Sensory-motor perceptions and cognition are thus indissolubly linked to each other. The starting point of this relationship is the interaction between the individual and the environment, with no separation between subject and object (Olivetti Belardinelli 1986). The mental representations generated from this interaction are active

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7.83 6.02

processes including also motor components. That is, the transition from perception to cognition involving the collapse of probabilistic mental activity in discrete representations does not occur until the motor planning is translated in motor performance (Spivey 2007). Accordingly, mental imagery well embodies the pre-motor

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feed-forward control in the psychological system of human beings.

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