An fMRI investigation on image generation in different sensory modalities: The influence of vividness
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 and 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 et al., 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 (Algom and Cain, 1991, Carrasco and Ridout, 1993, Decety and Michel, 1989, Halpern, 1988, Intons-Peterson, 1992, Kosslyn, 1980, Kosslyn et al., 1978, Parsons, 1994, Shepard and Metzler, 1971), others state that these representations rely on abstract symbols of the sort used in language (Anderson and Bower, 1973, Pylyshyn, 1973, Pylyshyn, 1979, Pylyshyn, 1981, Pylyshyn, 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 et al., 2005, D’Esposito et al., 1997, Ishai et al., 2000a, Jahn et al., 2004, Mellet et al., 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 et al., 2005, Cui et al., 2007, Kosslyn et al., 1995, Kosslyn et al., 1999), auditory (Bunzeck et al., 2005, Hoshiyama et al., 2001), tactile (Yoo et al., 2003), olfactory (Bensafi et al., 2007, Djordjevic et al., 2005), gustatory (Kikuchi et al., 2005, Kobayashi et al., 2004), and kinaesthetic (Dechent et al., 2004, Lotze et al., 1999, Porro et al., 1996, Roth et al., 1996, Szameitat et al., 2007) imagery. Interestingly, a previous fMRI study from our group (Olivetti Belardinelli et al., 2004b, Olivetti Belardinelli et al., 2004a) 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 et al., 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.
Section snippets
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.
Stimuli
Subjects were stimulated with a set of 96 (12 for each category)
Image preprocessing
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
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 gyrus (BA37) was found for all the imagery modalities. The somatic imagery yielded also the activation of the right
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
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
References (84)
- et al.
Negative BOLD differentiates visual imagery and perception
Neuron
(2005) - et al.
Scanning silence: Mental imagery of complex sounds
NeuroImage
(2005) - et al.
Vividness of mental imagery: Individual variability can be measured objectively
Vision Research
(2007) - et al.
Comparative analysis of actual and mental movement times in two graphic tasks
Brain Cognition
(1989) - et al.
Is the human primary motor cortex involved in motor imagery?
Cognitive Brain Research
(2004) - et al.
A functional MRI study of mental image generation
Neuropsychologia
(1997) - et al.
Functional neuroimaging of odor imagery
NeuroImage
(2005) - et al.
Neurophysiological correlates of mental imagery in different sensory modalities
International Journal of Psychophysiology
(1997) - et al.
Regional cerebral blood flow patterns in visual imagery
Neuropsychologia
(1989) - et al.
Regional cerebral blood flow patterns related to verification of low- and high imagery sentences
Neuropsychologia
(1992)
Neural networks for internal reading and visual imagery of reading: A PET study
Brain Research Bulletin
Distributed neural systems for the generation of visual images
Neuron
The representation of temporal information in perception and motor control
Current Opinion in Neurobiology
Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging
NeuroImage
Mental imagery in motor context
Neuropsychologia
Proprio-tactile integration for kinaesthetic perception: An fMRI study
Neuropsychologia
Functional imaging of gustatory perception and imagery: “top-down” processing of gustatory signals
NeuroImage
Neural substrates of animal mental imagery: Calcarine sulcus and dorsal pathway involvement – An fMRI study
Brain Research
Neural correlates of topographic mental exploration: The impact of route versus survey perspective learning
NeuroImage
The assessment and analysis of handedness: The Edinburgh inventory
Neuropsychologia
Motor imagery of complex everyday movements. An fMRI study
NeuroImage
A neural basis for category and modality specificity in semantic knowledge
Neuropsychologia
Remembered odors and mental mixtures: Tapping reservoirs of olfactory knowledge
Journal of Experimental Psychology: Human Perception and Performance
Human associative memory
Perceptual symbol systems
Behavioural and Brain Sciences
Grounded cognition
Annual Review of Psychology
Grounding symbolic operations in the brain’s modal systems
Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception
Journal of Neurophysiology
The distribution and functions of mental imagery (Contribution to Education, No. 26)
Functional anatomic studies of memory retrieval for auditory words and visual pictures
The Journal of Neuroscience
Olfactory perception and olfactory imagery: A multidimensional analysis
Journal of Experimental Psychology: Human Perception and Performance
The mind’s nose: Effects of odor and visual imagery on odor detection
Psychological Science
Is there an inner nose?
Chemical Senses
The neural basis of mental imagery
Assessing the influence of scanner background noise on auditory processing. II. An fMRI study comparing auditory processing in the absence and presence of recorded scanner noise using a sparse design
Human Brain Mapping
Statistics of mental imagery
Mind
Mental navigation along memorized routes activates the hippocampus, precuneus, and insula
NeuroReport
Olfactory and visual mental imagery
Journal of Mental Imagery
Reported auditory imagery and its relationship with visual imagery
Journal of Mental Imagery
Mental scanning in auditory imagery for songs
Journal of Experimental Psychology: Learning, Memory and Cognition
Verbal coding in olfactory versus nonolfactory cognition
Memory and Cognition
Cited by (116)
Visual mental imagery: Evidence for a heterarchical neural architecture
2024, Physics of Life ReviewsImagery, emotion, and bioinformational theory: From body to brain
2023, Biological PsychologyBrain structural changes in blindness: a systematic review and an anatomical likelihood estimation (ALE) meta-analysis
2023, Neuroscience and Biobehavioral ReviewsOlfactory metacognition and memory in individuals with different subjective odor imagery abilities
2022, Consciousness and CognitionSelf-reported vividness of tactile imagery for object properties and body regions: An exploratory study
2022, Consciousness and CognitionCitation Excerpt :Nevertheless, there is evidence for mental imagery in other modalities, including for touch. For example, studies have investigated imagery for tactile patterns (Schmidt et al., 2014), object properties (Belardinelli et al., 2009; Klatzky et al., 1991; Newman et al., 2005; Uhl et al., 1994), tactile stimulation on a body site (Chivukula et al., 2021; Schmidt & Blankenburg, 2019; Yoo et al., 2003) and somatosthetic sensations (Belardinelli et al., 2009; Grebot & Paty, 2005) as well as affective touch (Lucas et al., 2015; Panagiotopoulou et al., 2018). To date, the results of a number of neuroimaging studies (fMRI, EEG) have shed light on the neural correlates of tactile imagery (Belardinelli et al., 2009; Chivukula et al., 2021; Fallgatter et al., 1997; Schmidt et al., 2014; Uhl et al., 1994; Yoo et al., 2003).
Visual mental imagery: Inside the mind's eyes
2022, Handbook of Clinical Neurology