1 Department of Physiology, School of Medicine, University of Santiago de Compostela, Santiago de Compostela, Spain, 2 Service of Ophthalmology, Complejo Hospitalario Universitario de Santiago de Compostela, Santiago de Compostela, Spain, 3 Service of Neurosurgery, Complejo Hospitalario Universitario de Santiago de Compostela, Santiago de Compostela, Spain and 4 Service of Clinical Neurophysiology, Complejo Hospitalario Universitario de Santiago de Compostela, Santiago de Compostela, Spain
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Abstract |
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Key Words: fusiform gyrus humans random dot stereograms stereopsis subdural recording
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Introduction |
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Cortical activation associated with stereopsis in humans was mostly studied by using functional magnetic resonance imaging (fMRI). These studies basically show that stereoscopic stimuli produces weak or variable activity in areas V1, V2, V3 and MT, strong activity in area V3A, V7 and posterior IPS, and stronger activity in V4d-topo, whereas more complex objects produce activity in the lateral occipital cortex (LO) and the fusiform gyrus (Kwee et al., 1999; Mendola et al., 1999
; Backus et al., 2001
; Gilaie-Dotan et al., 2001
; Nishida et al., 2001
; Iwami et al., 2002
; Tsao et al., 2003
). Scalp visual evoked potentials have also been used to study stereopsis (Braddick and Atkinson, 1983
; Norcia and Tyler, 1984
), but this technique has limited spatial resolution and therefore it is not appropriate to identify cortical visual areas. On the contrary, subdural electrodes have high spatial and temporal resolution. The implant of subdural electrodes in patients undergoing evaluation for surgery therefore offers a unique opportunity to examine how sensory information is processed throughout the various sensory pathways and how it reaches conscious perception. This technique combined with evoked potential recordings has been used to study several aspects of sensory cortical functions in humans (Ray et al., 1999
; Grunwald et al., 2003
; Mundel et al., 2003
).
The goal of the study reported here was to determine whether some cortical regions from the occipital and temporal lobes are involved in disparity processing, a requirement needed to achieve stereopsis. For this, we studied the cortical visually evoked responses to RDS recorded from subdural electrodes in a patient who suffered from occipital epilepsy. To our knowledge this is the first report to address this question that uses this recording technique combined with RDS in humans.
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Materials and Methods |
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The visual stimuli were projected by a computer-controlled standard multimedia projector onto a frontoparallel flat surface facing the subject at a distance of 115 cm. RDS were used as stimulus to study disparity sensitivity. They were generated by using a conventional personal computer running software developed in our own laboratory (Gonzalez and Krause, 1994). The patient wore red/green eyeglasses and viewed the frontal surface where the RDS were projected. To obtain a separate viewing for each eye red and green dot patterns were used. The picture viewed by each eye was a rectangular area made up of a matrix of 320 x 200 pixels subtending 38.8 x 24° of visual field (Background in Fig. 2). To generate the RDS, 10% of pixels were bright and 90% were dark. The patient had to fixate a small target with both eyes (0.36 x 0.36°, Fixation target in Fig. 2) located in the center of the screen. For evoking cortical potentials, all dots within an area of 1.2 x 1.2° centered within the left hemifield (x = 1.7°, y = 0°; Figure in Fig. 2) were shifted in opposite directions producing various negative (crossed) and positive (uncrossed) horizontal disparities. The disparity was maintained for a period of 275 ms. Repetitive disparity presentations were made every 2 s. When the disparity was present a small square was perceived either in front (negative disparity) or behind (positive disparity) the background, whereas with zero disparity no figure was perceived. Disparities ranging from +0.75 to 0.75° were used. Both dynamic (frame change every 1/60th s) and static RDS were used to assess disparity sensitivity. The luminance was 18.0 cd/m2 for the random dot fields (10% bright pixel density). After filtered by the eyeglasses, the luminance was 2.2 cd/m2 for the red pattern and 1.43 cd/m2 for the green pattern.
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Recordings started 2 days after the electrodes were implanted and were made for three consecutive days. Direct inspection of the patient was continuously made to ensure the reliability of the procedure. The patient reported to perceive the central Figure (Fig. 2) in front or behind the Background whenever negative or positive disparity was present in both static and dynamic RDS.
Evoked potentials were recorded from pairs of subdural electrodes by using standard equipment (Viking IV IOM; Nicolet Biomedical Ltd, Wisconsin) from electrodes 23, 34 and 56 of the BOT strip, 34 and 48 of the MO strip, and 12, 34, 56 and 78 of the LOTP grid (Fig. 1). The remaining electrodes did not allow reliable recordings. The recording of the electrode potential started 250 ms before the onset of the stimulus and lasted for 1 s. The trigger for starting each recording was produced by the same computer that generated the visual stimulus. The responses evoked by 100 consecutive stimulus presentations were averaged to obtain a final evoked potential for each type of stimulation. We used a 1 kHz high pass filter and 100 Hz low pass filter (American Electroencephalographic Society, 1986). Electrode impedance was <3 k
. The resulting averaged evoked potentials were then analyzed for the presence of deflections related to stimulus responses.
The experiments were conducted in compliance with the relevant laws and guidelines of the Bioethical Committee of our institution. The patient was fully informed about the objectives, details, and risks of the experiment and a written consent was obtained before the recordings documented in this report were made.
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Results |
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Responses to RDS were found in those recordings made from electrodes 23 of the BOT strip and 48 of the MO strip. Talairach (Talairach and Tournoux, 1988) coordinates (x, y, z) were (34, 50, 14) for electrode BOT-2, (49, 55, 16) for electrode BOT-3, (3, 65, 14) for electrode MO-4 and (3, 87, 2) for electrode MO-8. We shall refer to these areas as fusiform and pericalcarine areas, respectively. The recordings made from the remaining electrodes including those from the LOTP array (Fig. 1) did not show detectable responses to disparity.
As Figure 3 shows, recordings made in the fusiform area clearly show a prominent response for a disparity of +0.25°, whereas the remaining disparities evoked either a weaker response or no response at all. The evoked potential peaked at 210 ms after the stimulus onset, but there was no response to the stimulus offset. In the pericalcarine area every disparity produced both onset and offset potentials (Fig. 4). In this case the peak of the response occurred at
150 ms after the stimulus onset and offset respectively.
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Discussion |
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We also found responses to static RDS in the pericalcarine area. These responses may be due to the pattern change caused by the onset and offset of the disparity and not by the disparity itself. We cannot determine this because we were not able to measure responses to dynamic RDS from this array.
The responses to RDS we found in the fusiform area were disparity dependent whereas in the pericalcarine area were not (see Figs 3 and 4). One explanation for this finding is that the responses in the pericalcarine area were due to pattern change and not to disparity. Another possible explanation is that subdural electrodes averaged population activity across several disparity columns. In monkeys, at single-cell level, there is disparity sensitivity in areas V1, V2, V3 and V3A (Poggio et al., 1985, 1988
; Gonzalez et al., 1993
; Durand et al., 2002
; Prince et al., 2002
); however, disparity sensitivity changes within a few hundred microns. Subdural electrodes do not have enough spatial resolution to detect the disparity selectivity of small cellular clusters and therefore record the activity of a large population of cells simultaneously responding to several disparities and to pattern change. It may be possible that in the fusiform area cells related to positive and negative disparity are arranged in larger patches which can cause the electrodes to record responses selective to a given disparity.
Response latencies to the stimulus onset in the fusiform area peak at 210 ms, whereas in the pericalcarine area they peak at
150 ms. This longer response delay found in the fusiform area is indicative of a higher level in the processing of the visual information. Whereas responses to RDS in the pericalcarine area may be partially caused by pattern changes, this is not the case for the fusiform area. As shown in Figure 3, there is no response to zero disparity nor to most of the tested disparities. This indicates that in this area, the responses we found are caused by the disparity present in the stimulus and not by pattern changes. Moreover, when we used dynamic RDS we recorded similar responses as when we used static RDS (Fig. 3). Further evidence is shown in Figure 5. The upper part of the figure shows the responses to a static RDS with crossed and uncrossed disparities when the patient wore red/green glasses. Note that the elicited response is present only when the figure was perceived behind the background. The lower part of Figure 5 shows the response to the same stimuli when the patient did not wear the eyeglasses and therefore no depth was perceived. In this case the potential was similar in amplitude and shape for both disparities. It is interesting to observe that the morphology of the evoked potential changed, suggesting that disparity triggers a specific pattern of activation of the cell population in the fusiform area.
Correlated and uncorrelated RDS evoke similar responses in the pericalcarine area, while in the fusiform area only correlated RDS produce responses. This finding suggests that this later area represents a high level of the processing of retinal disparities. As Figure 6 shows, while uncorrelated RDS produce clear on- and offset responses in the pericalcarine area, they do not produce any response in the fusiform area. Single-cell responses to uncorrelated stereograms have been reported in early stages of the visual pathways such as areas V1, V2 and V3V3A of the monkey (Poggio et al., 1988; Gonzalez et al., 1993
). It is assumed that at some stage in the hierarchy of the visual areas, the neural mechanisms for disparity selectivity must achieve stereo correspondence by exhibiting selectivity only for correlated random dot stereograms. Although it is likely that the stereo correspondence problem is not achieved solely in the fusiform area, in our study we provide evidence for an area in which this problem may have been solved. This is in agreement with the finding that in monkeys the end-stage of the ventral visual pathway for stereopsis may be the lower bank of the rostral superotemporal sulcus, known as area TEs (Janssen et al., 2003
).
We observed that for RDS, while there was a strong response from the contralateral hemifield only a weak and delayed response was obtained from the ipsilateral hemifield (Fig. 7). Single unit recording studies in monkeys indicate that cells from the IT cortex have receptive fields that are larger than in more posterior areas of the ventral visual pathway, that respond stronger at the foveal position and that prefer the contralateral hemifield above the ipsilateral hemifield (Schwartz et al., 1983; Komatsu and Ideura, 1993
; Tovee et al., 1994
; Logothetis et al., 1995
; Missal et al., 1999
; Op De Beeck and Vogels, 2000
). The preference of IT cells for contralateral stimulation agrees with our observation that the stronger response was obtained from the contralateral hemifield. Thus, at this stage, although most of the stereoscopic processing may already be solved, both hemifields are not yet fully combined. We believe that this may happen at hierarchically higher cortical areas.
It has been suggested that the 3D features of objects are processed in the parietal areas, which belong to the dorsal visual system (Shikata et al., 1996; Sakata et al., 1997
). Recently, neurons and regions related to binocular disparity have been found in the IT cortex, which is part of the ventral visual pathway, of monkeys (Janssen et al., 1999
, 2003
; Uka et al., 2000
). These neurons are selective for disparity-defined 3D shapes and in the vast majority of them the selectivity depends on the global binocular disparity gradient and not on the local disparity, indicating a high level of stereoprocessing (Janssen et al., 1999
). Our findings support the involvement of the ventral pathway in processing stereoscopic information.
Address correspondence to Dr Francisco Gonzalez, Department of Physiology, School of Medicine, E-15782 Santiago de Compostela, Spain. Email: francisco.gonzalez{at}usc.es.
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Acknowledgments |
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