Visual mental imagery during caloric vestibular stimulation
Introduction
The vestibular system plays a fundamental role in human spatial orientation. For example, it activates the vestibulo-spinal reflexes needed to control posture and affects gaze via the vestibulo-ocular reflex (VOR). The VOR connects the vestibular end-organ to the eye muscles in such a way that moving the head in one direction induces a compensatory eye movement in the opposite direction. This reflex helps stabilize the image of the world on the retina, when we move our heads. Furthermore, vestibular information is used, when we perceive the orientation of objects (e.g., with respect to gravity, Mittelstaedt, 1983), and it continuously updates the internal representation of space (e.g., Berthoz, Israel, Georges-Francois, Grasso, & Tsuzuku, 1995).
Numerous neuroimaging studies of the human vestibular system have now been reported, some of which have shown that early visual cortex is deactivated during vestibular stimulation (Bense, Stephan, Yousry, Brandt, & Dieterich, 2001; Deutschländer et al., 2002; Wenzel et al., 1996). This result is consistent with findings reported by Tiecks, Planck, Haberl, & Brandt (1996), who, using Doppler sonography, found that vestibular stimulation reduces blood flow in the posterior cerebral artery, which supplies the occipital cortex. Brandt, Bartenstein, Janek, & Dieterich (1998) and Brandt et al. (2002) interpreted this finding as reflecting an inter-sensory interaction that helps prevent sensory conflicts (e.g., eliminates distracting visual information caused by retinal slip during vestibular stimulation). In fact, researchers have also documented the complementary pattern, a deactivation of vestibular areas during visually induced self-motion (Brandt et al., 1998; Deutschländer et al., 2004) and visual fixation (Naito et al., 2003). These findings are consistent with those from psychophysical studies that show increased thresholds for detecting body acceleration during visually induced body motion (Probst, Straube, & Bles, 1985).
The present study took advantage of the finding that vestibular stimulation deactivates the occipital cortex in order to study visual mental imagery. Many neuroimaging studies of visual mental imagery have shown that early visual areas, including area 17, are activated, when people form detailed, high-resolution visual mental images (for review, see Kosslyn & Thompson, 2003). However, neuroimaging is essentially a correlational technique. Although one transcranial magnetic stimulation study did show that deactivating medial occipital cortex impairs imagery (Kosslyn et al., 1999), this finding does not demonstrate deactivation via natural mechanisms of sensory integration and would, therefore, be more compelling if buttressed by convergent evidence using natural stimulation and entirely different techniques (cf. Pylyshyn, 2002, Pylyshyn, 2003). If early visual areas are in fact deactivated during vestibular stimulation, and high-resolution visual imagery relies on such areas, then we expect to find impaired performance in high-resolution imagery during such stimulation.
Moreover, we had a second reason for studying mental imagery during vestibular stimulation. Neuroimaging studies have revealed activation in parietal cortex during certain imagery tasks, particularly those involving mental rotation (Alivisatos & Petrides, 1997; Cohen et al., 1996; Kosslyn, DiGirolamo, Thompson, & Alpert, 1998; Richter et al., 2000). It is noteworthy that some of the areas found to be engaged in mental rotation tasks are also activated, when people perceive rotation during vestibular stimulation (e.g., the intra-parietal sulcus; Lobel, Kleine, Bihan, Leroy-Willig, & Berthoz, 1998; Lobel et al., 1999). Therefore, it is likely that such processing may be affected by vestibular stimulation. However, based on previous research, it is possible that simultaneous vestibular stimulation might not interfere, but rather could act to facilitate mental rotation. This alternative is supported by the report that mental imagery deficits following hemispatial neglect can be temporarily attenuated by vestibular stimulation (Rode & Perenin, 1994; Rode, Perenin, & Boisson, 1995). This finding suggests that vestibular information is important in constructing a representation of space, and hence vestibular stimulation conceivably could facilitate spatial imagery tasks.
Thus, our goal was to investigate the mechanisms shared by visual mental imagery and vestibular processes. We elicited a relatively constant vestibular response, while participants performed either a high-resolution mental imagery task, a mental rotation task, or a control task that did not require imagery, but instead required participants to evaluate statements about abstract entities. We did not expect vestibular stimulation to affect performance of the control task. In this study, we employed caloric stimulation to elicit vestibular stimulation. Caloric stimulation occurs, when a cold or warm temperature is applied to the outer ear canal, which in turn induces a thermoconvection within the fluid of the horizontal semicircular canal (Barany, 1906; Formby & Robinson, 2000). This stimulates the horizontal semicircular canal of the vestibular system as if the head were actually rotating.
Section snippets
Participants
Eight volunteers participated (five males and three females, ages 24–42 years) in two separate sessions. They received monetary compensation. Each participant was tested clinically and was verified to have normal vestibular and oculo-motor functions. None of the participants reported any history of vestibular problems or disease. This study was approved by the Institutional Review Boards at the Massachusetts Eye and Ear Infimary and Harvard University.
High-resolution mental imagery
The participants began by memorizing 40
Results
First, we consider the analysis of the error rates (ERs). We conducted a 3 (task type: high-resolution mental imagery, mental rotation, low-mental-imagery sentences) × 2 (stimulation type: sham, caloric) ANOVA with both task type and stimulation type as repeated measures and ER as the dependent variable. There was no main effect of task, F < 1, and no main effect of stimulation per se, F < 1. Thus, the error rates suggest that the tasks were of comparable difficulty. However, the two variables
Discussion
The results indicate that participants perform two types of mental imagery tasks poorly, when they experience simultaneous vestibular input via caloric stimulation. In contrast, they performed a low-imagery task as well with and without caloric stimulation, which indicates that the observed effects did not reflect overall impaired cognitive performance during caloric stimulation.
Perhaps the most important result of this study is that caloric stimulation impaired performance in the
Acknowledgments
We thank Molly Crockett and Dwight Channer for expert technical assistance, and Csilla Haburcakova and Jason Tsajima for their assistance in testing the participants. We are also grateful to William Thompson for providing helpful advice in designing the study and Conrad Wall and the Jenks Vestibular Diagnostic Laboratory for providing the caloric irrigator. This research was supported by NIH/NIDCD Grant R01 DC04158 (DMM) and NIH Grant 1 R01 MH60734-01 (SMK), NSF Grant ROLE (SMK), NIMA Grant
References (62)
- et al.
Functional activation of the human brain during mental rotation
Neuropsychologia
(1997) - et al.
Remission of hemineglect and anosognosia during vestibular stimulation
Neuropsychologia
(1987) Mental rotation and the right hemisphere
Brain & Language
(1997)- et al.
Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging
Neuroimage
(2002) - et al.
Brain areas underlying visual imagery and visual perception: An fMRI study
Cognitive Brain Research
(2004) - 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) - et al.
Four types of mental imagery processing in upright and tilted observers
Cognitive Brain Research
(2003) - et al.
Visual mental images can be ambiguous: Insights from individual differences in spatial transformation abilities
Cognition
(2002) - et al.
Differential effects of ambivalent visual–vestibular–somatosensory stimulation on the perception of self-motion
Behavioral Brain Research
(1985)
Return of the mental image: Are there pictures in the brain?
Trends in Cognitive Sciences
Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging
Cognitive Brain Research
Neural systems activated during visual mental imagery: A review and meta-analyses
Untersuchungen über den vom vestibular apparat des Ohres reflektorisch ausgelösten rythmischen Nystagmus und seine Begleiterscheinungen
Monatsschrift für Ohrenheilkunde
Adaptation in the oculomotor response to caloric irrigation and the merits of bithermal stimulation
British Journal of Audiology
Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI)
Journal of Neurophysiology
Spatial memory of body linear displacement. What is being stored?
Science
Identification of the central vestibular projections in man: A positron emission tomography activation study
Experimental Brain Research
Cerebral representations for egocentric space: Functional–anatomical evidence from caloric vestibular stimulation and neck vibration
Brain
Reciprocal inhibitory visual–vestibular interaction: Visual motion stimulation deactivates the parieto-insular vestibular cortex
Brain
PsyScope: A new graphic interactive environment for designing psychology experiments
Behavior Research Methods, Instruments, and Computers
Changes in cortical activity during mental rotation: A mapping study using functional MRI
Brain
Sensory system interactions during simultaneous vestibular and visual stimulation in PET
Human Brain Mapping
Rollvection versus linearvection: Comparison of brain activations in PET
Human Brain Mapping
Dominance for vestibular cortical function in the non-dominant hemisphere
Cerebral Cortex
Mental rotation and orientation-invariant object recognition: Dissociable processes
Cognition
Measurement of vestibular ocular reflex (VOR) time constants with a caloric step stimulus
Journal of Vestibular Research
Neuronal responses in the parieto-insular vestibular cortex of alert Java monkeys (Macaca fascicularis)
Localization and responses of neurons in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis)
Journal of Physiology
Unilateral neglect restricted to visual imagery
Nature
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