Brain Advance Access originally published online on May 6, 2004
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Brain, Vol. 127, No. 6, 1393-1402, 2004
© 2004 Guarantors of Brain
doi: 10.1093/brain/awh158
Accurate bidirectional saccade control by a single hemicortex
Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada
Correspondence to: Daniel Guitton, Montreal Neurological Institute, 3801 University Street, Montreal, Quebec, Canada H3A 2B4. E-mail: dguitt{at}mni.mcgill.ca
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Anatomical, electrophysiological and lesion studies indicate that each cortical hemisphere normally generates saccades directed to the contralateral side. In contrast, in patients who had an entire cortical hemisphere removed surgically (hemidecortication), the remaining hemicortex can generate both contraversive and ipsiversive saccades. However, current evidence indicates that ipsiversive saccades are grossly inaccurate. The obvious reason for this is that hemidecorticate patients are blind in the hemifield ipsilateral to the remaining hemicortex, and therefore normal visual signals are not available to drive ipsiversive saccades. However, absent vision also implies that visual error signals are not available to calibrate ipsiversive movements. Furthermore, the innate anatomical substrate needed to support accurate ipsiversive saccade control, in addition to the normal contraversive control, appears sparse. We show here that, in spite of these obstacles, hemidecorticate patients could generate accurate ipsiversive saccades in a task that dissociated hemianopia from saccade direction. In this task, while the patients fixated a central fixation target (FT), saccade targets (STs) were briefly presented to the intact visual hemifield contralateral to the intact hemicortex. The FT was then moved towards and beyond the former location of the ST which evoked tracking eye movements that moved the eyes towards and then beyond the ST, thereby moving the goal, ST, into the blind visual hemifield ipsilateral to the intact hemicortex. When the FT was extinguished, the patients generated, in the dark, ipsiversive saccades that moved their eyes to the remembered location of the ST with the same accuracy as normal control subjects. This indicates that a single hemicortex can mediate accurate bidirectional saccade control via fully functional bilateral connections from cortex to brainstem oculomotor structures. The mechanisms whereby visual signals can calibrate ipsiversive saccades remain elusive.
Key Words: hemidecorticate patients; cerebral hemispherectomy; saccades; visuospatial representation; plasticity
Abbreviations: EOG= electrooculography; FEP = final eye position; FT = fixation target; SRT = saccade reaction time; ST = saccade target
Received June 11, 2003. Revised February 8, 2004. Accepted February 8, 2004.
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Introduction |
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Anatomical and physiological studies in monkeys as well as lesion studies in both humans and monkeys have led to the concept that each cortical hemisphere controls voluntary saccadic eye movements directed contralaterally (reviewed in Leigh and Zee, 1999
; Pierrot-Deseilligny et al., 2002). In contrast to this widely accepted belief, there is evidence that each hemicortex has the innate capacity to generate both ipsiversive and contraversive saccades. Electrical microstimulation of the cerebral cortex may evoke ipsiversive as well as contraversive saccades in both humans (Penfield and Jasper, 1954) and monkeys (Schlag and Schlag-Rey, 1987; Dassonville et al., 1992; Tehovnik and Lee, 1993; Thier and Anderson, 1998; Mushiake et al., 1999). Human patients with unilateral cerebral cortical lesions may exhibit deficits for both ipsiversive and contraversive saccades (Guitton et al., 1985; Pierrot-Deseilligny et al., 1987, Pierrot-Deseilligny et al., 1991a, b; Braun et al., 1992; Rivaud et al., 1994). Furthermore, following the complete transection of the corpus callosum (callosotomy), the key fibre bundle connecting the two cortical hemispheres, saccades can be generated to both the left and right in response to instructional colour cues presented to only a single hemicortex (Hughes et al., 1992).
Perhaps the most convincing evidence for cortical control of bidirectional saccades is that voluntary saccades can be generated to both the left and right following the removal of an entire cortical hemisphere (hemidecortication) (Bruell and Volk, 1956; Troost et al., 1972a; Perenin and Jeannerod, 1978; Sharpe et al., 1979; Estanol et al., 1980; Tusa et al., 1986). While it may be tempting to credit these remarkable capabilities to the development of new pathways caused by long-term preoperative disorders, this view is inadequate because recovery of the control of bidirectional saccades has been observed within 1–2 weeks following hemidecortication in juvenile monkeys that were completely normal preoperatively (Tusa et al., 1986). This suggests that innate bidirectional saccade control may be subserved by existing bilateral connections from each hemicortex to important subcortical oculomotor centres including the superior colliculus (Leichnetz et al., 1981; Distel and Fries, 1982; Shook et al., 1990), nucleus reticularis tegmenti pontis (Leichnetz et al., 1984; Huerta et al., 1986; Stanton et al., 1988) and the paramedian pontine reticular formation (Leichnetz et al., 1984; Schnyder et al., 1985; Huerta et al., 1986; Stanton et al., 1988; Shook et al., 1990).
It remains unresolved, however, whether a single hemicortex has normal accurate control of saccades directed ipsilateral to itself or whether only crude control is possible. To date, studies of callosotomy (Hughes et al., 1992) and hemidecorticate (Bruell and Volk, 1956; Troost et al., 1972a; Perenin and Jeannerod, 1978; Sharpe et al., 1979; Estanol et al., 1980) patients have not demonstrated that a single hemicortex can generate accurate ipsiversive saccades. In fact, both hemidecorticate human patients (Troost et al., 1972a; Estanol et al., 1980) and monkeys (Tusa et al., 1986) generate grossly inaccurate saccades to visual targets presented ipsilateral to their intact hemicortex. Clearly, there are major impediments to the control of accurate ipsiversive saccades by hemidecorticate human patients. First and most obvious is that the complete absence of visual cortical structures on the decorticate side prevents the necessary visual processing required to generate a saccade directly to a visual target; the patients are hemianopic (Stoerig and Cowey, 1997). Secondly, monkey studies suggest that innate crossed corticofugal connections are sparse (Leichnetz et al., 1981, 1984; Distel and Fries, 1982; Schnyder et al., 1985; Huerta et al., 1986; Stanton et al., 1988; Shook et al., 1990). Thirdly, hemianopia may remove the visual error signals necessary for calibrating the amplitude of ipsiversive saccades (Wallman and Fuchs, 1998; Noto and Robinson, 2001; Seeberger et al., 2002).
To investigate ipsiversive saccade control, we studied two patients who had undergone hemidecortication in order to cure chronic life-threatening epileptic seizures (Villemure and Rasmussen, 1993). We tested whether the patients could generate accurate saccades directed ipsilateral to their intact hemicortex when a target was presented briefly to their intact (contralateral) hemifield and then transferred to their blind (ipsilateral) hemifield by intervening eye movements generated in complete darkness. The results were compared with those results obtained when the remembered target location was not transferred between hemifields as well as with the results of four normal control subjects. Preliminary results have been presented as an abstract (Herter et al., 1998).
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Subjects
One complete right hemidecorticate patient (D.R.) and one partial right hemidecorticate patient (S.E.) participated in this study which was approved by the Montreal Neurological Institute and Hospital Research Ethics Committee. The cortical ablations performed on D.R. and S.E. are illustrated in Fig. 1 and the case histories of these patients are described in Table 1. Both D.R. and S.E. underwent hemidecortication to relieve intractable epilepsy associated with hemianopia and hemiparesis. D.R. underwent a complete functional hemidecortication of the right side at 17 years of age. This procedure involved removal of the temporal lobe, including mesial structures, and a frontal–parietal corticectomy. A few remaining cortical regions were left in situ, but were disconnected from the remaining brain by completely sectioning the underlying white matter. S.E. underwent a partial hemidecortication of the right side at 25 years of age. This procedure involved a temporal–parietal–occipital lobectomy, including mesial structures. The entire right frontal lobe was spared as was the anterior parietal lobe. Note that S.E. had suffered life-long hemiparesis indicating that, although the entire frontal lobe was spared, the motor cortex on the decorticate side was dysfunctional. At the time of this study, D.R. and S.E. were 24 and 32 years of age, respectively, and were seizure free and unmedicated. More complete case histories and surgical details have been published previously (Tomaiuolo et al., 1997
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Four normal control subjects ranging from 22 to 32 years of age also participated in this study. Data from three of the four normal subjects were collected and published as part of a previous study that used the same task (Herter and Guitton, 1998
). None of the normals had any history of neurological or psychiatric disorders. All subjects gave informed and voluntary consent prior to commencement of experimentation.
Apparatus
Subjects were seated in complete darkness with their heads restrained by a chin rest and bite bar. They faced a matt-black cylindrical screen located at a constant distance of 50 cm from their eyes along the horizontal meridian. Two visual targets, a fixation target (FT) and a saccade target (ST), that could appear horizontally at any location between ±30° were used for the experiments. Each target was generated by a red laser beam (0.5° diameter, 670 nm, 12.0 cd/m2) that was front-projected onto the screen using servo-controlled mirrors (General Scanning).
Experimental paradigm
The paradigm consisted of three tasks (Fig. 2). In the transfer task (Fig. 2A), the subjects generated saccades to the remembered location of the ST after it had been transferred between visual hemifields by eye movements used to track the FT toward and then beyond the remembered location of the ST. The non-transfer task (Fig. 2B and C) was an interleaved control task that was similar to the transfer task, except that the remembered location of the ST remained within the same hemifield as its initial presentation. In half the non-transfer trials, tracking eye movements were directed toward, but not beyond, the remembered location of the ST (Fig. 2B), while, in the other half of the non-transfer trials, tracking eye movements were directed in the opposite direction to the remembered location of the ST (Fig. 2C). Because tracking in half of the non-transfer trials was in the same direction as tracking in the transfer trials, the subjects could not predict, at the start of tracking, whether an ipsiversive or contraversive saccade would be required. Finally, the flash task [delayed memory-guided saccade task (Hikosaka and Wurtz, 1983)] was an interleaved control task in which no tracking eye movements were generated, though delays between target presentation and saccade onset were matched (Fig. 2D).
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The subjects initiated each trial by pressing a button, which resulted in the central (0°) presentation of an FT, which the subjects were instructed to look at (fixate). After 1000 ms, an ST was flashed for 100 ms at a horizontal location randomly selected from ±10, ±20 and ±30° while the subjects continued to look at the FT. For transfer and non-transfer trials, 400 ms after the ST was extinguished, the FT moved at a constant velocity of 10°/s either toward (A and B) or away from (C) the remembered location of the ST. Subjects were instructed to follow (track) the FT with their eyes until the FT was extinguished after a randomly determined displacement of 10, 20 or 30°. For flash trials (D), after the ST was extinguished, the FT remained stationary at the centre for another 1400, 2400 or 3400 ms (matched delays) before it was extinguished. The end of a trial occurred 2000 ms after the FT was extinguished and was signalled by a short sound. Thus, for all trials,
the subjects were given 2000 ms to look (saccade) to the remembered location of the ST and maintain their gaze steady (fixate) at that location. Note that, for the flash task only, the ST was relit for 2000 ms at the end of each trial. As all trials were carried out in complete darkness, other than the FT and ST, there were no visual cues available to help the subjects accurately saccade to the ST.
The paradigm was organized into blocks of 108 trials, 36 transfer trials, 36 non-transfer trials (18 with ipsi- and 18 with contraversive tracking) and 36 flash trials. As the ST was presented in equal numbers to both hemifields, each block contained 18 trials to each hemifield in each task. D.R. completed five blocks for a total of 90 trials in each task to each hemifield. S.E. completed six blocks for a total or 108 trials in each task to each hemifield. The three normals who had participated in our previous study (Herter and Guitton, 1998) had completed one block each, while the fourth normal completed six blocks.
Recording of eye movements
Horizontal eye position was measured using bitemporal electrooculography (EOG) obtained from two Ag–AgCl skin electrodes placed bitemporally and a third ground electrode placed in the middle of the forehead. To minimize drifts and noise, the skin was cleaned thoroughly at the point of contact with the electrode. Furthermore, the subjects wore the electrodes for at least 20 min in complete darkness before calibration and recording. This served to reduce fluctuations in the DC offset. Small drifts were corrected for by automatically resetting the EOG output to zero as the subjects fixated the FT at the start of every trial. With these methods, the subjects could be quickly prepared and tested in sessions that could last 3 h (with rest periods) while maximizing their comfort. Furthermore, when properly calibrated and guarded against drifts, the EOG signal was accurate within ±1° over a range of ±30° for all subjects, which was sufficient for our needs.
For each subject, the EOG signal was calibrated at least every 15 min during each testing session by having the subjects fixate a target that jumped predictably from 0° to +20° to 0° to –20° to 0°. This target displacement sequence was repeated while the gain of the EOG signal was adjusted manually to assure a fixed output voltage for the 20° target offset. During the course of testing, the calibration of the EOG signal was also verified by relighting the ST for 2000 ms following each trial of the flash task. When necessary, experiments were interrupted in order to recalibrate the gain of the EOG signal.
The experimental paradigms and collection of eye position data were controlled by a 486 PC computer running version 5.4 of the REX real time data acquisition system (Hays et al., 1982). Eye position data were stored to hard disk at a rate of 1000 Hz and subsequently filtered and analysed on PC workstations running Matlab version 5.3 (The Mathworks). Eye position signals were filtered digitally using a low-pass finite impulse response filter with a 30 Hz cut-off frequency that was applied both forwards and backwards, resulting in zero phase distortion.
Data analysis
Data were analysed for all trials except those in which: (i) the horizontal eye position deviated further than ±2.5° from the FT during the interval from 500 ms after its onset until it moved; (ii) the horizontal eye position deviated further than ±5° from the FT while it was moving; or (iii) EOG signals contained significant drifts, noise or blink artefacts (determined by visual analysis). As previous studies have shown that hemidecorticate patients tend to generate a staircase-like sequence of several saccades in order to attain targets (Troost et al., 1972a; Estanol et al., 1980), we included up to five saccades in our data set for each trial (trials with more than five saccades were not included in further analyses). Using horizontal eye velocity obtained from a five-point moving differential of horizontal eye position, the onset and end of each putative saccade were found as those points where velocity increased above and decreased below 30°/s, respectively. The duration, amplitude and peak velocity were then obtained and the saccade was accepted if the duration was <500 ms, the amplitude exceeded 1° and the maximum velocity exceeded 80°/s.
Quantitative analysis of final eye position (FEP), end-point error and saccade reaction time (SRT) were carried out using analyses of variance (ANOVA) with repeated measures across the three tasks (transfer, non-transfer and flash) and two of the ST positions (10 and 20°). FEP was calculated as the horizontal eye position at the end of each trial (2000 ms after the FT was extinguished). End-point error was defined as the absolute difference between mean FEP and ST position. SRT was calculated as the time between FT offset and the onset of the first saccade in each trial. Note that the 30° ST position was not included in the ANOVAs because the paradigm did not permit transfer trials with the ST at 30°. For each patient, within-subject effects were analysed using the mean values for each block that the patients completed. For comparisons between the patients and normals, between-group effects were analysed using the overall means for all blocks. When necessary, pairwise comparisons were made using the Bonferroni correction.
Similar to previous studies of normal monkeys (McKenzie and Lisberger, 1986; Schlag et al., 1990) and humans (Ohtsuka, 1994; Zivotofsky et al., 1996; Herter and Guitton, 1998), we also carried out quantitative comparisons (t tests) between correlations of overall gaze shift amplitude with two diametrically opposed potential behavioural outcomes, spatiotopic amplitude and retinotopic amplitude. The overall gaze shift amplitude was calculated as the difference between the FEP and horizontal eye position before the first saccade after the FT was extinguished. Spatiotopic amplitude was calculated as the difference between the ST position and horizontal eye position at the onset of the first saccade after the FT was extinguished. Retinotopic amplitude was calculated as the position of the ST relative to the centre, i.e. relative to where the FT was located when the ST was shown briefly at the start of a trial.
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Here we present only those trials in which the ST was presented to the intact visual hemifield (contralateral to the intact hemicortex), where the ST was clearly seen.
Saccade accuracy
Figure 3 illustrates, for each combination of task and ST position, the mean FEP generated by D.R. (Fig. 3A), S.E. (Fig. 3B) and the normals (Fig. 3C). It is evident for both D.R. and S.E. that, in the transfer task (black bars), saccades generated ipsiversive to the intact hemisphere were generally as accurate as or, in some cases, more accurate than contraversive saccades generated in the non-transfer and flash tasks (grey and white bars). Statistical analyses revealed that end-point error did vary marginally across tasks for both D.R. [F(2,8) = 3.72, P = 0.07] and S.E. [F(2,10) = 3.23, P = 0.08]. Pairwise comparisons between each task revealed that end-point error was smaller in the transfer task than the non-transfer and flash tasks in both D.R. and S.E., though significant differences were not found except in S.E. where end-point error was significantly less in the transfer task than in the flash task (P < 0.05).
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It is also evident in Fig. 3 that the mean FEP of both patients was consistently less than that of the normals. Interestingly, the end-point error of the patients tended to be less than that of the normals because the latter overshot the target position. However, in spite of these differences, statistical analyses failed to find significant differences between the patients and normals for either mean FEP [F(1,4) = 4.16, P > 0.1] or mean end-point error [F(1,4) = 1.13, P > 0.1].
It is of interest to consider how the multiple saccades that the patients generated per trial (Fig. 2, see next section) improved their accuracy relative to their first saccade. On average, D.R.’s end-point error at the end of each trial was reduced, relative to that at the end of the first saccade, by 0.9, 5.3 and 5.5° in the transfer, non-transfer and flash tasks, respectively. On average, S.E.’s end-point error at the end of each trial was reduced, relative to that at the end of the first saccade, by 2.1, 5.1 and 4.3° in the transfer, non-transfer and flash tasks, respectively. Thus, additional saccades conferred an advantage in both subjects, though that advantage was less in the transfer task than in the non-transfer and flash tasks.
Figure 4 compares, for all tasks and conditions, the relationship between overall gaze shift amplitude and, respectively, spatiotopic amplitude (Fig. 4A–C) and retinotopic amplitude (Fig. 4D–F). The linear regression equations are given in Table 2 for each task and condition. We found that overall gaze shift amplitude consistently was better correlated (P < 0.05) with spatiotopic amplitude than with retinotopic amplitude for D.R. (Fig. 4A and D), S.E. (Fig. 4B and E) and the normals (Fig. 4C and F) for the transfer task (black dots), the non-transfer task with contraversive tracking (white dots), and for the non-transfer task with ipsiversive tracking (grey dots). This implies that they compensated for the eye movements that intervened between target presentation and saccade onset rather than basing their responses on the initial retinal position of the target. It is also of particular interest that, in the transfer task (black dots in Fig. 4), the correlation between overall gaze shift amplitude and spatiotopic amplitude in the patients was not significantly different from that in the normals (P > 0.1; Table 2).
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Number of saccades
Table 3 shows a breakdown of the number of saccades per trial that the patients generated in order to move their eyes to the ST. We failed to find a significant difference across tasks with regards to the number of saccades that the patients had generated at the end of a trial [D.R. F(2,8) = 0.67, P > 0.1; S.E. F(2,10) = 1.99, P > 0.1]. However, although the overall accuracy of the patients’ saccades was similar to that of the normals, the number of saccades that the patients had generated at the end of a trial was significantly higher than the normals [F(1,4) = 28.14, P < 0.01].
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Saccade reaction times
Figure 5 illustrates the mean SRT in each task for D.R. (black lines) and S.E. (white lines), as well as the range of mean SRT for the normals (grey shading). It is evident that, for both D.R. and S.E., the mean SRT was not longer for ipsiversive saccades generated in the transfer task than for contraversive saccades generated in the non-transfer task. In the case of S.E., the mean SRT did not differ significantly between tasks [F(2,10) = 0.00, P > 0.1]. In the case of D.R., mean SRT differed significantly between tasks [F(2,8) = 5.03, P < 0.05] because mean SRT was actually marginally lower in the transfer task compared with the flash task (P = 0.1). It is also evident that, for each task, the mean SRTs for both D.R. and S.E. were within the range of the mean SRT for the normals. Furthermore, we failed to find a significant difference between the mean SRT of the patients and the normals [F(1,4) = 0.04, P > 0.1].
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Discussion |
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We have shown that in the absence of direct visual guidance, patients D.R. and S.E. could generate accurate saccades that compensated for eye movements that intervened between the brief presentation of a visual target to the intact visual hemifield and the subsequent targeting saccade. This ability was remarkably similar for saccades that were contraversive and ipsiversive relative to the remaining hemicortex, and did not depend on whether tracking eye movements were contraversive or ipsiversive. It was particularly interesting that ipsiversive saccades were highly accurate, because each hemicortex is thought normally to drive contraversive saccades. It is also interesting that the performance of S.E. was no better than that of D.R. even though S.E. had a spared frontal lobe, while D.R. had a complete hemidecortication. This emphasizes the remarkable ability of one hemicortex to perform this difficult task.
Compensation for intervening eye movements
Hallett and Lightstone (1976) originally demonstrated that humans have the ability to generate spatially accurate saccades that compensate for intervening saccadic eye movements generated in the absence of external visual cues. More recently, the ability to compensate for intervening pursuit eye movements has been demonstrated in normal monkeys (Schlag et al., 1990) and humans (Ohtsuka, 1994; Zivotofsky et al., 1996; Herter and Guitton, 1998). This ability is believed to require an efference copy (or corollary discharge) of the motor commands used to generate all intervening changes in gaze direction (Guthrie et al., 1983; Lewis et al., 2001). For saccades, it appears that this corollary discharge is transmitted by the thalamus to the cortex where it is used to update the mental representation of visuomotor space, i.e. the relative positions of both targets and gaze within the surrounding environment (Gaymard et al., 1994; Sommer and Wurtz, 2002).
Within the cortex, maintenance of this accurate representation of visuomotor space appears to occur within the posterior parietal cortex because patients with posterior parietal lesions, particularly on the right side, are impaired in their ability to compensate for intervening saccades directed ipsilaterally and contralaterally to the lesion, the deficit being particularly worse for the latter (Duhamel et al., 1992; Heide et al., 1995). In contrast, in our patients, the remaining left hemicortex was able to maintain an accurate representation of visuomotor space by accurately monitoring their tracking eye movements, irrespective of direction. This ability may not be too surprising because hemidecorticate patients are known to track smoothly moving targets, with saccades when target movement is directed contralateral to the intact hemicortex and with smooth pursuit when target movement is directed ipsilateral to it (Troost et al., 1972b; Sharpe et al., 1979; Estanol et al., 1980; Tusa et al., 1986). Such tracking ability falls within the normal function of a hemisphere, because each hemicortex normally controls ipsiversive smooth pursuit and contraversive saccades (reviewed in Leigh and Zee, 1999). However, while true for S.E., this principle did not strictly hold for D.R., who generated contraversive tracking that combined both saccades and smooth pursuit, each movement contributing about equally to overall eye displacement (Table 4). Given that D.R. was remarkably able to compensate for contraversive tracking (Figs 2A and B, 3A and 4A), it follows that the intact hemicortex of this patient may have acquired some ability to generate and monitor contraversive smooth pursuit.
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Calibration of saccade gain
In the transfer task, the patients were able to adjust accurately the amplitude of saccades directed ipsilateral to the intact hemicortex. Given that visual feedback is required in order to calibrate the amplitude gain of saccades to visual targets (Wallman and Fuchs, 1998
; Noto and Robinson, 2001; Seeberger et al., 2002), it is intriguing that the patients had acquired the ability to calibrate the gain of ipsiversive saccades (into their blind hemifield). We can only speculate that in everyday life, this could occur during behaviour analogous to the transfer task when two stimuli, at different angular distances from the fovea and located contralateral to the intact hemicortex (in the intact hemifield), are selected as targets. In this case, calibration would occur in the process of refining the accuracy of a sequence of saccades that takes the eyes to the furthest target first and then to the target nearest the initial fixation point. Alternatively, we speculate that calibration could also occur during saccades to multimodal (visual and auditory) stimuli that are heard within the blind hemifield, but not seen until after the saccade is generated.
Implications regarding brain organization
Our observations show that a single hemicortex can generate saccades in both directions and that ipsiversive saccade control can be very accurate. This accuracy and the similar SRTs observed in all three tasks suggest that the patient’s intact hemicortex has fully functional bilateral connections with brainstem oculomotor structures. Indeed, innate bilateral connections from the cortex have been observed to the superior colliculus (Leichnetz et al., 1981; Distel and Fries, 1982; Shook et al., 1990), nucleus reticularis tegmenti pontis (Leichnetz et al., 1984; Huerta et al., 1986; Stanton et al., 1988) and the paramedian pontine reticular formation (Leichnetz et al., 1984; Huerta et al., 1986; Stanton et al., 1988; Shook et al., 1990). Furthermore, an increased number of crossed connections from cortex to the superior colliculus have been observed following experimental hemidecortication in cats (Adelson et al., 1995). This may explain why the superior colliculus remains anatomically intact on the decorticate side following experimental hemidecortication in monkeys (Theoret et al., 2001). Bilateral involvement of the superior colliculus is supported further by another observation showing that our hemidecorticate patients can generate short-latency ‘express saccades’ to auditory targets ipsilateral to their intact hemicortex (Reuter-Lorenz et al., 1999), a function that normally requires the superior colliculus (Schiller et al. 1987).
Conclusions
We conclude that a single hemicortex has the adaptive capacity to generate bidirectional saccades and monitor bidirectional tracking. Perhaps this occurs due to the expansion of innate, but sparse, bilateral connections into fully functional connections from cortex to brainstem oculomotor structures.
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Acknowledgements |
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We wish to thank the subjects, in particular D.R. and S.E., for their participation, Dr A. Ptito for providing us with the patients, their MRIs and their case histories, Dr I. Armstrong for helping with statistical analysis, Drs A. Ptito, M. Ptito and J. Fecteau for valuable discussions, and Mr J. Roy and Mr J. Knowles for technical support. This research was supported by a research grants from the Canadian Institute of Health Sciences (CIHR) and the Fonds de la Recherche en Santé du Québec (FRSQ) Réseau Vision to D.G. T.M.H. was the recipient of a CIHR studentship.
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