Visual mental imagery during caloric vestibular stimulation

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Abstract

We investigated high-resolution mental imagery and mental rotation, while the participants received caloric vestibular stimulation. High-resolution visual mental imagery tasks have been shown to activate early visual cortex, which is deactivated by vestibular input. Thus, we predicted that vestibular stimulation would disrupt high-resolution mental imagery; this prediction was confirmed. In addition, mental rotation tasks have been shown to activate posterior parietal cortex, which is also engaged in the processing of vestibular stimulation. As predicted, we also found that mental rotation is impaired during vestibular stimulation. In contrast, such stimulation did not affect performance of a low-imagery control task. These data document previously unsuspected interactions between the vestibular system and the high-level visual system.

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

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