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The Role of Area 17 in Visual Imagery: Convergent Evidence from PET and rTMS

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Science  02 Apr 1999:
Vol. 284, Issue 5411, pp. 167-170
DOI: 10.1126/science.284.5411.167

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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.

Many people report that they visualize when they recall information about the shape, color, or texture of an object that was encoded only incidentally, when they reason about space, understand descriptions of scenes, and so on. Although these reports are not in dispute, what they signal about mental processes has been a thorny problem for centuries (1). One issue focuses on whether the experience of visualization is a hallmark of an internal representation that depicts shapes. Such a “depictive” representation is extended in space and represents each part of an object so that the distances among the parts in the representation correspond to the distances among the corresponding parts of the object. The activation of topographically organized areas of visual cortex during visual mental imagery has been taken as evidence that such representations are present (2). However, it is possible that such activation is a nonfunctional byproduct of activation in other areas and itself plays no actual role in representing information during imagery. Here we demonstrate that the activation in topographically organized cortex engendered by an imagery task underlies processing used to carry out that task.

Numerous neuroimaging experiments have investigated the neural underpinning of imagery by the use of various techniques, including positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). The results of these studies are mixed, but about half of the studies have found activation during visual imagery in medial occipital cortex (corresponding to either Area 17 or 18, both of which are topographically organized in the human brain), whereas the remaining studies did not find such activation (3). The experiments differ in many ways, ranging from the nature of the task to the specific neuroimaging techniques used, and thus there are many possible reasons for the disparities. One way that the studies differ is in the requirement that subjects actually must form a depictive image (4).

In this investigation we used a task that clearly requires one to visualize patterns that depict information. Moreover, we investigated the same task with PET and repetitive transcranial magnetic stimulation (rTMS), showing not only that Area 17 is activated when people perform the task, but also that performance of this task is impaired when neural activity in this region of cortex is disrupted by rTMS.

We used the imagery task designed by Kosslyn, Sukel, and Bly (5). Eight subjects (6) memorized a display that contained four quadrants, each of which contained a set of stripes (Fig. 1). The subjects were scanned as they closed their eyes and visualized the display (7), and then heard two numbers, which they had previously learned were labels for specific quadrants, followed by the name of a dimension (such as “length”). They were to decide whether the set of stripes in the first-named quadrant was greater along that dimension than the set of stripes in the second-named quadrant. The resulting brain activation was compared with a control condition in which the same type of auditory stimuli were delivered but no imagery was used (8).

Figure 1

Illustration of stimuli used in the task. All sets of stripes together were about 5 inches high and 5 inches wide (subtending ∼13° of visual angle from the subject's point of view). As illustrated, the stripes varied in length, width, orientation, and the amount of space between the bars. The numbers 1, 2, 3, and 4 were used to label the four quadrants, each of which contained a set of stripes. After memorizing the display, the subjects closed their eyes, visualized the entire display, heard the names of two quadrants, and then heard the name of a comparison term (for example, “length”); the subjects then decided whether the stripes in the first-named quadrant had more of the named property than those in the second. Subjects were told to make their judgments by visualizing the stripes.

The PET data were analyzed with publicly available statistical parametric mapping software (9). The key result was that we found activation in Area 17 (Fig. 2). Other areas were also activated, including Areas 18/19 (Fig. 2), but they are not relevant for the present issue (10).

Figure 2

The results of PET scanning, showing activation in Area 17 [peak Z score of 3.38 at coordinates −2, −88, −12, according to the Talairach and Tournoux atlas (23)], during imagery compared with baseline. Activation in Areas 18/19 (peak Z score of 3.44 at coordinates 34, −86, 12) can also be seen in this slice plane. Strength of Z scores is illustrated according to color, with blue, green, yellow, and red representing increasingly highZ scores; in this slice plane, the highest Zscore, located within Area 17, is 3.31.

Neuroimaging can only establish the association between task performance and a pattern of cortical activation. In contrast, by transiently disrupting the function of a targeted cortical region, rTMS allows one to test the causal link between activity in that region and task performance (11). This technique essentially creates a temporary, reversible “lesion”; this lesion need only be severe enough to produce observable decrements in performance. In 1989, Amassian et al. (12) demonstrated that single pulses of transcranial magnetic stimulation (TMS) delivered to the occipital cortex 60 to 140 ms after a visual stimulus disrupt performance on a letter-identification task. Since then, the suppressive effects of single-pulse TMS on visual cortex have been replicated in various experiments (13). Such single-pulse studies require both temporal and spatial knowledge: where to stimulate and when. In contrast, rTMS can modulate the level of excitability of a given cortical area beyond the duration of the rTMS train itself, thereby providing an opportunity to test the contribution of that cortical area to a given task without stringent temporal constraints (14). For example, after being delivered at a rate of 1 Hz, rTMS decreases cortical excitability for minutes afterward (15), thereby providing a transient, partial “functional lesion” of a specific cortical region and allowing one to test its causal link to performance in a task.

Using 1-Hz real or sham rTMS (16), we stimulated five subjects (17) over the occipital pole, targeting Area 17 (18). Real or sham rTMS was applied before performance of an imagery or a perceptual version of the task used in the PET study (19–21). In the perceptual version of the task subjects compared the sets of stripes on a visible display. If we did not succeed in disrupting perception in the same task, we would have little evidence that we had interfered with the function of the visual cortex per se. As shown in Fig. 3, TMS delivered to medial occipital cortex did in fact disrupt both perception and imagery.

Figure 3

Results when rTMS was delivered before the imagery and perception conditions. “Real” rTMS occurred when the magnetic field was directed into Area 17, whereas “sham” rTMS occurred when the field was diverted away from this site. A two-way repeated analysis of variance (ANOVA) on the response times (trimmed to eliminate outliers) revealed a main effect of stimulation (real rTMS versus sham rTMS) [F (1,4) = 29.86,P < 0.01] and a main effect of modality (imagery versus perception) [F (1,4) = 16.65, P < 0.02)]. There was no interaction between stimulation and modality [F(1,4) < 1]. Contrasts revealed that the response times during real rTMS were greater than those during sham rTMS in both imagery [F (1,4) = 9.32, P < 0.04] and perception [F (1,4) = 8.17, P < 0.05] (1945 ms versus 1759 ms and 1002 ms versus 827 ms, respectively). As shown here, this response time increase was observed in all five subjects in both modalities. Digits next to each line indicate subject number. The corresponding ANOVA on the error rates revealed no significant effects (all F's < 1, allP's > 0.5), which belies the possibility of a speed-accuracy trade-off (the means were as follows: sham perception, 13.3%; real perception, 13.3%, sham imagery, 9.2%; real imagery, 13.3%). The error rates during the TMS condition were lower than in the PET condition, which probably reflects the large number of practice trials used here versus the small number used in the PET study. For PET, we wanted the task to be as challenging as possible, thereby engendering maximal blood flow in relevant brain areas, but for rTMS we wanted to ensure that response times were not at ceiling, and thus included many more practice trials.

Real, compared with sham, rTMS targeted toward the subject's Area 17 led to impaired performance in both the perceptual and the imagery tasks. In the PET experiment we found multiple cortical areas activated, but previous research has shown that stimulating one visual area does not disrupt processing in other areas that are similar distances from the site at which TMS was directed (22).

In summary, we not only found that medial occipital cortex, specifically Area 17, was activated while people visualized and compared sets of stripes, but also that such activation was not “epiphenomenal” (that is, akin to the heat produced by a lightbulb when one is reading, which plays no functional role in allowing one to read). The TMS results show that the activation revealed by PET is indeed causally linked to performance of the task, that the early occipital visual cortical areas are indeed used in at least some forms of visual imagery as well as in visual perception.

  • * To whom correspondence should be addressed. E-mail: smk{at}wjh.harvard.edu

  • Present address: Service de Neurologie et de Neuropsychologie, C.H.U. Hôpital de la Timone, Marseille, France.

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