The Role of Area 17 in Visual Imagery: Convergent Evidence from PET and rTMS
10.1126/science.284.5411.167
Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

Visual imagery is used in a wide range of mental activities, ranging from memory to reasoning, and also plays a role in perception proper. The contribution of early visual cortex, specifically Area 17, to visual mental imagery was examined by the use of two convergent techniques. In one, subjects closed their eyes during positron emission tomography (PET) while they visualized and compared properties (for example, relative length) of sets of stripes. The results showed that when people perform this task, Area 17 is activated. In the other, repetitive transcranial magnetic stimulation (rTMS) was applied to medial occipital cortex before presentation of the same task. Performance was impaired after rTMS compared with a sham control condition; similar results were obtained when the subjects performed the task by actually looking at the stimuli. In sum, the PET results showed that when patterns of stripes are visualized, Area 17 is activated, and the rTMS results showed that such activation underlies information processing.

Bibliography

Kosslyn, S. M., Pascual-Leone, A., Felician, O., Camposano, S., Keenan, J. P., L., W., Thompson, Ganis, G., Sukel, K. E., & Alpert, N. M. (1999). The Role of Area 17 in Visual Imagery: Convergent Evidence from PET and rTMS. Science, 284(5411), 167–170.

Authors 10
  1. S. M. Kosslyn (first)
  2. A. Pascual-Leone (additional)
  3. O. Felician (additional)
  4. S. Camposano (additional)
  5. J. P. Keenan (additional)
  6. W. L. (additional)
  7. Thompson (additional)
  8. G. Ganis (additional)
  9. K. E. Sukel (additional)
  10. N. M. Alpert (additional)
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  14. Before the imagery condition subjects memorized the stimulus display [using the procedure of (5)]. They also learned which quadrants were labeled by the numbers 1 2 3 and 4. During the imagery task the subjects were asked to visualize the entire display and then listen to the stimuli. If the stripes in the quadrant named first had a pattern that was greater on the named dimension than the stripes in the quadrant named second they were to press the pedal under their left foot; if not the pedal under their right foot. Subjects were told that they should visualize the entire display and “look” at the image in order to make the discrimination. They were to respond as quickly and accurately as possible. Subjects received two practice trials (with feedback regarding accuracy which was not provided in the actual test trials) before the actual test trials. We wanted to ensure that the task was difficult and hence likely to evoke detectable activation and thus did not include many practice trials. Each block lasted about 85 s: subjects began the task 15 s before delivery of 15 OCO 2 began and continued for 70 s at which point the PET camera was turned off and subjects were instructed to stop performing the task. All other aspects of the procedure were the same as in (5). The mean response time in the imagery condition was 2704 ms and the mean error rate was 21.5%.
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  33. Repetitive TMS was performed with a Magstim Super Rapid stimulator (Magstim Whitland UK) with a Magstim Double 70-mm figure-of-eight coil. The coil was firmly maintained in a constant position with a specially designed coil holder. A three-dimensional reconstructed MRI of each subject was used to determine the optimal coil placement to target the occipital pole at the tip of the calcarine fissure. During real rTMS the center of the coil was held tangentially to the scalp and symmetrically across the midline of the occipital pole targeting the tip of the calcarine fissure. During sham rTMS the coil was lowered by 3 cm and rotated so that the edge of the two wings of the coil rested at 90° on the scalp. In this sham rTMS condition the induced magnetic field did not enter the brain although the touch on the scalp the sound of the coil being activated and the induced muscle twitching are comparable to those in the real rTMS condition. Intracerebral measurements of the induced voltages by TMS with various coil orientations in primates document the appropriateness of the sham TMS condition used here [
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  35. ]. Repetitive TMS was delivered at 90% of the subject's motor threshold at 1-Hz stimulation frequency in a single train of 10 min duration. Our hypothesis was that underlying cortical activity would be affected for at least 10 min after rTMS. To avoid carry-over effects between conditions there was a pause of 30 min between tasks and thus between rTMS trains. Overall each subject received 600 stimuli per train and a total of 2400 stimuli (1200 real and 1200 sham stimuli). Stimulation was performed in accordance with current safety recommendations [
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  39. Although it remains unclear whether the effects of TMS to the occipital pole are due to direct intracortical effects or interference with connections from the affected area functional disruption of Area 17 is well documented (12). Nevertheless given the limitations in focality of TMS interference with contiguous portions of Area 18 is likely [see for example
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  42. The same task as in the PET experiment was administered [see (5)] and subjects again were asked to respond as quickly and accurately as possible (by pressing two different keys with the middle and index finger of their dominant hand). Response time was measured from the time of stimulus onset to the key response; error rates were also measured. Subjects learned the stimulus display as before. However because response times and error rates were our only dependent measures we included 24 practice trials before the study to ensure that there would not be a ceiling effect; if the task was too challenging it would have been difficult to detect differences among the conditions.
  43. The same task was used in the imagery and perception conditions but in the perception condition the entire stimulus display appeared for 500 ms immediately after the auditory cue was presented. Before each experimental task (imagery or perception) sham or real rTMS was applied. The subject received rTMS while sitting in front of the computer to be used for testing (Macintosh 17-inch RGB monitor Apple Computer Cupertino CA). The task was initiated immediately after the end of the last magnetic stimulus. Therefore each subject received a total of four sessions of rTMS. To control for potential learning effects the subjects were randomly assigned to receive sham ( n = 2) or real rTMS ( n = 3) first. The imagery task was always conducted first to prevent the subjects from overlearning the stimuli (and thus not having to use imagery later) which may have occurred if the perceptual task was presented first.
  44. Repetitive TMS was tolerated well by all subjects without undesirable side effects. No pre- or post-TMS differences in neurological status or visual acuity were noted in any of the subjects. None reported phosphenes during the stimulation.
  45. For example G. Beckers and V. Homberg [ Exp. Brain Res. 87 421 (1991)] and G. Beckers and S. Zeki [ Brain 118 49 (1995)] showed that TMS over the presumed site of Area V5 impaired motion perception but left color perception and shape perception unchanged; in contrast TMS to V1 (Area 17) disrupted detection of visual stimuli without affecting motion perception. Areas V5 and V1 are interconnected and therefore if the effects of TMS on a given cortical area were secondary to transsynaptic effects TMS to V1 should disrupt motion perception (by remote effects onto V5) and TMS to V5 should disrupt visual perception in general (by remote effects onto V1). This was not the case. Although transsynaptic effects of TMS on distant cortical and subcortical areas are possible [for example (10.1093/brain/118.1.49)
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  48. ] these effects have not been found to produce significant changes in behavior within the time span studied here. TMS effects appear to originate from disruption of the same cortical areas that show activation on functional imaging studies and originate primarily from disruption of the directly targeted cortical region. Among the areas activated in our study [see (10)] the one closest to Area 17 (where TMS was delivered) was Areas 18/19 which was at a distance of 43.3 mm; the closest other areas that were activated were the cerebellum 43.7 mm from Area 17 and the occipito-parietal sulcus 45.3 mm from Area 17. Given the previous findings with TMS noted above it is unlikely that TMS delivered to medial occipital cortex had its effects by disrupting one of the more remote areas that were activated during the task.
  49. J. Talairach and P. Tournoux Co-planar Stereotaxic Atlas of the Human Brain M. Rayport transl. (Thieme New York 1988).
  50. This research was supported in part by grants from the Human Frontiers Science Program National Eye Institute (RO1 EY12091) and the National Institute for Mental Health (RO1 MH57980). S.C. was a visiting scientist from the Department of Pediatrics Division of Neurology Faculty of Medicine University of Chile. Subjects were tested according to American Psychological Association rules and regulations. After the general purpose and possible risks of the experiment were explained informed consent was obtained from each subject before the experimental procedure began. This research was approved by the respective Institutional Review Boards of the sponsoring institutions.
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 5:40 a.m.)
Deposited 1 year, 7 months ago (Jan. 13, 2024, 12:24 a.m.)
Indexed 3 days, 19 hours ago (Aug. 27, 2025, 11:33 a.m.)
Issued 26 years, 4 months ago (April 2, 1999)
Published 26 years, 4 months ago (April 2, 1999)
Published Print 26 years, 4 months ago (April 2, 1999)
Funders 0

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@article{Kosslyn_1999, title={The Role of Area 17 in Visual Imagery: Convergent Evidence from PET and rTMS}, volume={284}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.284.5411.167}, DOI={10.1126/science.284.5411.167}, number={5411}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Kosslyn, S. M. and Pascual-Leone, A. and Felician, O. and Camposano, S. and Keenan, J. P. and L., W. and Thompson and Ganis, G. and Sukel, K. E. and Alpert, N. M.}, year={1999}, month=apr, pages={167–170} }