Foveal Attention Modulates Responses to Peripheral Stimuli

Simo Vanni and Kimmo Uutela

Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, FIN-02015 HUT Espoo, Finland


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Vanni, Simo and Kimmo Uutela. Foveal Attention Modulates Responses to Peripheral Stimuli. J. Neurophysiol. 83: 2443-2452, 2000. When attending to a visual object, peripheral stimuli must be monitored for appropriate redirection of attention and gaze. Earlier work has revealed precentral and posterior parietal activation when attention has been directed to peripheral vision. We wanted to find out whether similar cortical areas are active when stimuli are presented in nonattended regions of the visual field. The timing and distribution of neuromagnetic responses to a peripheral luminance stimulus were studied in human subjects with and without attention to fixation. Cortical current distribution was analyzed with a minimum L1-norm estimate. Attention enhanced responses 100-160 ms after the stimulus onset in the right precentral cortex, close to the known location of the right frontal eye field. In subjects whose right precentral region was not distinctly active before 160 ms, focused attention commonly enhanced right inferior parietal responses between 180 and 240 ms, whereas in the subjects with clear earlier precentral response no parietal enhancement was detected. In control studies both attended and nonattended stimuli in the peripheral visual field evoked the right precentral response, whereas during auditory attention the visual stimuli failed to evoke such response. These results show that during focused visual attention the right precentral cortex is sensitive to stimuli in all parts of the visual field. A rapid response suggests bypassing of elaborate analysis of stimulus features, possibly to encode target location for a saccade or redirection of attention. In addition, load for frontal and parietal nodi of the attentional network seem to vary between individuals.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

During attention to one visual target, a parietofrontal attentional network is essential for search and selection of new targets (Corbetta et al. 1991; LaBerge 1995; Posner and Petersen 1990; Vanni et al. 1997). This search requires shifts of attention between objects or locations and shifts of gaze. In monkeys, functional areas participating in these functions are rather well known. The lateral intraparietal area (LIP) in the intraparietal sulcus and the frontal eye field (FEF) anterior to the arcuate sulcus have been mainly associated with planning and execution of saccades (Andersen 1989; Schall 1997). Both areas are sensitive to sensory stimuli, even without eye movements (Barash et al. 1991; Kodaka et al. 1997). The 7a in the inferior parietal lobule (IPL) participates in the spatial representation of the visual environment (Siegel and Read 1997). In addition, area 7a contains cells that are most sensitive to peripheral visual stimuli when visual attention is focused onto foveal targets (Mountcastle et al. 1981, 1987). These 7a neurons thus seem to monitor the nonattended visual field, an operation necessary for deciding where to attend or move the eyes next.

In humans, attentional and oculomotor tasks activate partially overlapping cortical areas. Strongest parietal activation can be found postcentrally and close to the intraparietal sulcus and frontal activation in the precentral frontal cortex (Corbetta 1998; Nobre et al. 1997). The monkey's LIP and 7a are most likely the homologues to these human parietal areas, whereas the frontal locus corresponds to monkey FEF. Although the locations of the human parietal and frontal areas involved in shifts of eyes and attention are relatively well characterized, sensitivity of these areas to nonattended sensory stimuli and the timing of their activation are still poorly known.

In some previous human studies, activation in the FEF was found when attention was directed to peripheral stimuli (Kim et al. 1999; Nobre et al. 1997; Vandenberghe et al. 1997). We measured neuromagnetic signals to peripheral luminance stimuli while attention was directed to a fixation point, released while maintaining fixation, and during longer periods of passive fixation. The peripheral luminance stimuli were never targets in the main experiment. In control experiments, precentral responses to visual stimuli were studied during an auditory task, and during attention to visual periphery. The aim of this study was to find out which areas are sensitive to nonattended peripheral stimuli during visual attention, and the timing of this enhancement. The main experiment followed a paradigm used in several monkey studies probing functions of the IPL (Motter and Mountcastle 1981; Mountcastle et al. 1981, 1987; Siegel and Read 1997). The visuospatial control experiment followed the paradigm of Steinmetz et al. (1994). A brief report of these results has appeared in an abstract form (Vanni and Uutela 1999).


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

We studied 11 right-handed healthy volunteers (5 females, 6 males, mean age 27.7 yr, range 22-36 yr). Figure 1 shows the experimental setup. The subjects fixated a small (0.3°) white (53 cd/m2) square with a dark center projected on a dark background (4 cd/m2) at 63 cm distance. First, the center of the fixation square (half of its width) increased in luminosity (fixation-on), and after a randomized 1- to 4-s interval the center dimmed (fixation-dimming) for 0.5 s before becoming dark again (fixation-off). A 12 × 6° rectangular luminance stimulus (53 cd/m2) was presented 10° off the fixation along the horizontal meridian, either left or right in random order. The stimulus appeared 1.5 s after the fixation onset and again 1.5 s after fixation dimming with a duration of 200 ms. If the fixation-dimming followed fixation-onset within 2 s (20% of the epochs), no stimulus was delivered.



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Fig. 1. Appearance and timing of the visual stimuli. Top line presents luminance in the center of fixation square. Increase of luminance indicated beginning of the trial, dimming the request for response, and dark center the intertrial period. Middle line shows the timing of the 200-ms luminance stimuli.

During the trials, the subjects focused their attention on the fixation square and lifted their right index finger when they detected its dimming. The dimming was adjusted to be barely detectable, and the subjects were encouraged to react as fast as possible. During intertrial intervals (3-s periods between 2 trials) the subjects waited for the fixation square to light up, which marked the beginning of the next trial. During passive viewing the subjects fixated the central square with no task while the peripheral luminance stimuli were presented. The passive viewing was measured in two separate blocks, one before and the other one after the active trial-intertrial measurement.

Signals were recorded with a Neuromag-122 whole-scalp neuromagnetometer that is equipped with planar gradiometers (Ahonen et al. 1993). Signals were filtered (pass-band 0.03-90 Hz), sampled at 300 Hz, and averaged time locked to the onset of the peripheral luminance stimulus. A ±8-ms jitter of the stimulus onset, due to asynchrony between the stimulus computer and the data projector, smoothed the averaged signals roughly as a 25-Hz low-pass filter. One hundred responses were averaged for each distinct file (6 files: trial, intertrial, and passive viewing for both the left and right visual fields).

To estimate the cerebral currents, the average signals were preprocessed by applying a 200-ms prestimulus baseline and a 40-Hz low-pass filter. We used the minimum current estimate (MCE) (Uutela et al. 1999), an implementation of the minimum l1-norm estimate. MCE explains most of the measured signals with a current distribution that has the smallest sum of current amplitudes. The estimate is calculated separately for each time point. The estimates were studied both as a group average over the subjects, to increase the signal-to-noise ratio and to easily detect the activation consistent across the subjects, and separately for each subject, to detect individual variability.

Active areas in the individual subjects were determined from the average of the three conditions (trials, intertrials, and passive viewing), separately for the left and right visual field stimuli. Regions of interest (ROIs) were selected to cover all steadily active areas within 400 ms from stimulus onset. The mean and extent of the ROIs were automatically adjusted to fit the estimated activity. The activity of the region was calculated as a weighted average of the estimate: the maximum weight was at the center of the ROI and extended to the neighboring locations with the form of a three-dimensional generalized normal distribution. The ROI was accepted for further study if its estimated activity during the response exceeded 2 nanoamperemeters (nAm) and twice the peak activity during prestimulus baseline, the duration exceeded 10 ms, and the active area seemed to be stationary. The coordinates of the centers of the ROIs were transformed to the Talairach and Tournoux (1988) coordinate system.

Group average of the estimates was calculated without taking orientation of the sources into account. The estimates were aligned based on three anatomic landmarks on the surface of the heads, and the results were shown on a standard brain volume (Roland et al. 1994). Selection criteria for the ROI were the same as for the individual subjects, but the three conditions were screened separately.

Evoked electroencephalographic (EEG) responses were recorded simultaneously with the magnetoencephalographic (MEG) recordings from 19 locations of the International 10-20 system and from the right mastoid, referred to left mastoid. For the study of the left hemisphere the signals referred to right mastoid were calculated off-line. Signals were filtered (pass-band 0.03-100 Hz), sampled at 300 Hz, and averaged time locked to stimulus onset.

Eight subjects participated in a separate saccade reaction time experiment. In the Saccade task, subjects made immediate saccades to a 1.5° square-shaped luminance stimuli when they appeared 11.5° left or right from the fixation in random order. The stimuli were presented for 400 ms and interstimulus interval was randomized from 1 to 28 s. In the Attention + Saccade task, subjects had to perform a dual task. First, they had to indicate transient luminance increments of the fixation with immediate finger lifts. In addition, they had to make immediate saccades when the peripheral luminance stimuli appeared. The luminance increments of the fixation appeared randomly at 1- to 4-s intervals, whereas the peripheral saccade targets had the 1- to 28-s intervals as in the Saccade task; the fixation and peripheral stimuli were at least 1 s apart from each other. Twenty saccades to both left and right targets were collected. The saccade onset latencies were calculated off-line from horizontal electrooculogram (EOG) signals.

Subjects 2 and 7 participated in two MEG control experiments. In an auditory attention task, the subjects viewed the same visual stimuli as in the main experiment, but the changes in fixation luminance were replaced by changes in tone frequency. Tones (500 Hz) were presented for 1-4 s binaurally at 40 dB above the hearing threshold, and the subjects had to detect a 200-ms 10-Hz frequency glide upwards at the end of the tone. There were 3-s intervals between the tones. Hence the tone and intertone intervals corresponded to the trial and intertrial intervals in the main experiment.

In a visuospatial task, the two subjects fixated a point while 6° square-shaped luminance stimuli were shown randomly to one of eight possible peripheral locations, 11.5° horizontally and/or vertically from fixation. Thus the distance between fixation and stimulus was either 11.5 or 16°. First, one location was cued by presenting a luminance stimulus for 400 ms. After the cue, one to five stimuli in other locations were delivered before the cued location was stimulated again. Subjects were asked to lift their right index finger after the end of the second stimulus at the cued location. If no response was delivered or it was delivered outside a 500-ms window after stimulus, the epoch was rejected. Subjects received immediate visual feedback about their performance, and the session continued until 100 responses at the cued locations were collected and averaged. Signals for the noncued stimuli were averaged separately.

The control studies were measured 1 yr after the main experiments with a new 306-channel Neuromag Vectorview neuromagnetometer. Signals were filtered (pass-band 0.03-200 Hz), sampled at 600 Hz, and averaged time locked to the onset of the peripheral luminance stimulus. In both the behavioral and MEG control experiments the stimuli were back-projected on a screen, and the viewing distance was 60-64 cm.

In all MEG experiments vertical and horizontal EOGs were recorded, and epochs contaminated with saccades or blinks were rejected on-line from the averaged signals. In addition to artifact rejection, the horizontal EOG signals were quantified off-line to reveal possible differences in eye movements between the experimental conditions. Epochs with horizontal EOG signals exceeding a low threshold were considered to include overt eye movements.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

In individual subjects the peripheral luminance stimulus evoked on average 12 distinct neuromagnetic responses. In the occipital lobe, middle, ventral, lateral, and superior (cuneus) parts were all activated in at least one-half of subjects at least by one hemifield stimuli. Similarly, inferior and superior temporal cortices and the temporooccipital border were commonly active. At the parietal lobe, inferior parietal lobulus and precuneus/parietooccipital regions were commonly active as well as the temporoparietal border. In the frontal cortex activation was common in the precentral and premotor cortices. Although both individual and group analysis showed clear signals in parietal lobes, the most systematic difference between the experimental conditions was found, to our surprise, in the right precentral region.

Figure 2A shows minimum current estimates for two subjects projected on triangular meshes covering their brain. Figure 2B shows the estimated locations of the right precentral activation projected on the surface of magnetic resonance images (MRIs). The estimated source location is between the central sulcus and precentral gyrus in both subjects. For subject 2, the center of the estimated location is on the precentral gyrus. For subject 7, the left visual field (LVF) activation is on the precentral gyrus, and the right visual field (RVF) activation is in the precentral sulcus. Figure 2B shows the source strengths as a function of time for the two hemifields during the trials. After the stimulus onset, the activation was strongest between 130 and 160 ms for subject 2 and between 120 and 150 ms for subject 7. Both subjects showed stronger activation for the contralateral stimulation, and subject 7 had 10-20 ms shorter latencies for the contralateral compared with ipsilateral stimuli. An offset response emerged between 300 and 400 ms in subject 7, whereas in subject 2 the possible offset response was close to baseline noise level.



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Fig. 2. A: minimum current estimates after left visual field stimuli. Samples between 130 and 150 ms are integrated for subject 2 and between 120 and 140 ms for subject 7. White lines surround currents projected on precentral cortices. B: location of the right precentral currents for the left and right visual field stimuli are projected on the surfaces of individual magnetic resonance (MR) images. C: precentral source strengths as a function of time during the trials.

Figure 3A shows the group average of the current distribution between 100 and 160 ms after the left visual field stimuli. Estimated activities for trial, intertrial, and passive viewing conditions are projected on the surface of the standard brain. The right precentral region shows the strongest activation during trials, clearly above the baseline noise level.



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Fig. 3. A: average neuromagnetic activity of all subjects 100-160 ms after the stimulus onset, projected on the surface of a standard brain volume. Circles mark the right precentral area containing more activity during trials than intertrials. B: activity in the right precentral region of interest (ROI) for the left and right hemifield stimuli as a function of time during the 3 conditions. Gray areas mark the time interval between 100 and 160 ms.

Figure 3B shows the estimated current in the right hemisphere precentral region as a function of time. The mean strength 100-160 ms after the left visual field stimulation was significantly stronger during the trials (1.4 ± 0.8 nAm, mean ± SD across subjects) than intertrials (0.7 ± 0.4 nAm, P < 0.005, Wilcoxon signed rank test) or during passive viewing (0.6 ± 0.3 nAm, P < 0.005). The corresponding values after the right visual field stimulation were 1.5 ± 0.8, 1.0 ± 0.6 (P < 0.05), and 0.8 ± 0.2 nAm (P < 0.005), respectively. When the right and left visual field responses were averaged, the right precentral region showed the strongest responses during trials in all subjects (P < 0.001 for both trial-intertrial, and trial-passive viewing comparisons, binomial test). The small amplitude values in the group analysis compared with individual analysis are due to inclusion of a time interval usually exceeding the individual active period, possible positional jitter in individual source location, and from the inclusion of subjects whose activity in this region was weaker than the individual criteria for applying a ROI.

Analysis of the individual datasets revealed right precentral or premotor activity fulfilling the source criteria in 6/11 subjects (Table 1). In line with the group average, individual activity was always strongest during the trial (P < 0.02, binomial test). Its mean (±SD) x, y, and z Talairach coordinates (Talairach and Tournoux 1988) were 49 ± 3, 0 ± 9, and 35 ± 8 mm. No systematic amplitude differences between the tasks were found in the left precentral region either in the group or individual analysis (source found in 6 subjects, coordinates -37 ± 8, -9 ± 11, and 43 ± 12 mm).


                              
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Table 1. Individual source latencies and strengths

The parietal lobes contained more sources and showed more individual variability than the precentral region; no significant differences between the stimulus conditions were found in the group data. Although functional areas cannot be distinguished based on the MR image only, we found some systematic features in the responses. Figure 4 shows estimated location of a right-hemisphere posterior parietal activation for six subjects. This source was found in 8/11 subjects and was mainly located inferior to the intraparietal sulcus and posterior to the supramarginal gyrus (Talairach coordinates 46 ± 6, -50 ± 9, 40 ± 5 mm). It was strongest on average at 180-220 ms; for timing of individual activity, see Table 1. In the left hemisphere an IPL source was present in five observers on average between 180-210 ms (x, y, and z coordinates -44 ± 6, 53 ± 18, and 31 ± 7 mm). The left IPL sources were located somewhat inferior to the right IPL sources, closer to the temporoparietal border.



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Fig. 4. Location of posterior parietal activity for 6 subjects, projected on the surface of individual MR images.

Individual analysis revealed possible functional differences between the subjects. For four subjects (boldface in Table 1), at least one hemifield stimulus evoked the right precentral cortex before 160 ms, and in two subjects after 210 ms; all six showed stronger responses during trials compared with the less attention demanding conditions. On the other hand, right inferior parietal lobule was active in eight subjects, but showed the strongest responses during trials in only four subjects (boldface in Table 1). Activation latencies in these four subjects were longer than 180 ms, and none of them showed precentral activation before 160 ms. The IPL and precentral responses were modulated in an interesting way in subjects with evoked activity in both of them. When the right precentral region was active later (after 210 ms, subject 1 RVF and subject 9 LVF), the right IPL responses during trials were enhanced, whereas when the right precentral region was active earlier (before 160 ms, both hemifields in subjects 2 and 7), the IPL responses during trials were not enhanced.

Figure 5 presents the dynamics of the right IPL and precentral activation in subject 1. The IPL source is transiently active around 200 ms, producing strongest signals during the trials. After this, the right precentral region reaches its maximum activity, and again the strongest signals are produced during trials. Although more right IPL than right FEF sources were found from individual data, a greater individual variability of IPL source locations might have hampered comparisons within the group average.



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Fig. 5. Parietal and frontal activity of subject 1 after right visual field stimulation. A: projection of active areas onto her brain surface; integrations over 2 consecutive time intervals are shown. B: temporal dynamics of the inferior parietal and precentral areas during trials, intertrials, and passive viewing. Gray area mark the time interval integrated for the images in A. Estimated locations of the parietal and frontal activations are projected onto the surface of her brain.

Magnetoencephalography may miss activity if the current is radial to the skull (Hämäläinen et al. 1993). To exclude radial activation as an explanation to missing differences between the experimental conditions, we recorded evoked potentials with 19 EEG channels simultaneously with the MEG recordings. Six subjects showed possible signal enhancement during trials between 100 and 250 ms in their dorsal right hemisphere or midline electrodes. From these, only one subject (subject 10, right visual field) had no simultaneous enhancement in right hemisphere IPL or precentral regions in his MEG recordings. Comparison of our MEG and EEG results suggests that the signal enhancement during trials is generated mainly in the fissural cortex, for which the MEG has the best sensitivity.

With two separate saccade experiments, we evaluated whether individual latency differences in MEG recordings are reflected in behavioral latencies. In the first task (Saccade) the subjects made saccades from fixation to a small peripheral luminance stimulus, appearing randomly in the left or right visual fields. In a second task (Attention + Saccade), subjects both had to indicate with finger lift transient luminance increments of the fixation point and make saccades to the peripheral luminance stimuli. Because the subjects with early right precentral enhancement (Frontal group, n = 4) showed the effect of attention on average ~60 ms earlier than the subjects with right IPL enhancement (Parietal group, n = 4) we presumed that saccade latencies should increase more in the Parietal group when subjects are attending the fixation. Figure 6 shows saccade latencies for the two tasks. During the Saccade-task, the mean (±SE) latencies were 354 ± 37 ms for the Frontal group and 309 ± 33 ms for the Parietal group. During the Attention + Saccade task the latencies were 390 ± 32 and 389 ± 58 ms, for the Frontal and Parietal groups. Thus attention to fixation seemed to extend saccade latencies on average 44 ms more in the parietal group, although this difference was not statistically significant (P = 0.057, 1-sided Wilcoxon rank-sum test).



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Fig. 6. Horizontal saccade latencies for Frontal and Parietal subject groups without (Saccade) and with (Attention + Saccade) a simultaneous task at the fixation point.

To specify the type of attention modulating the right precentral MEG response, we showed two subjects the visual stimuli of the main experiment (Fig. 1) during an auditory task. Subjects 2 and 7 participated in this study because they showed clear responses from both visual fields in the main experiment. Figure 7A shows activation within their right precentral ROI during the main experiment and Fig. 7B during the auditory attention control tasks. Subject 2 showed minor activation during auditory trials, but clearly less than during the original visual trials. During auditory intertrials no activation was present. She had, however, activation 2 cm posteromedially close to right central sulcus during both trials and intertrials. For subject 7, no precentral activation above noise emerged during this experiment.



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Fig. 7. Comparison of right precentral source strength as a function of time between the main and 2 control experiments. The ROI was determined from the main experiment data. Gray areas mark time intervals between 130 and 170 ms for subject 2 and between 110 and 155 ms for subject 7. A: main experiment with averaged responses to left and right visual field stimuli. B: auditory control experiment. Visual stimuli were identical to main experiment but attention was engaged in an auditory task. C: visuospatial control experiment. Visual stimuli appeared peripherally, either at an attended location (Targets) or in other locations (Nontargets).

With a visuospatial control experiment we wanted to find out whether the precentral response is present during attention to peripheral stimuli. Subjects 2 and 7 fixated a point and attended one of eight possible stimulus locations at a time. When stimuli appeared at nonattended locations (Fig. 7C), minor activation emerged for both subjects. When stimuli were attended, subject 2 showed no activation, whereas subject 7 showed strong activation. To clarify this result we relocalized the precentral ROIs from the control data.

Figure 8A displays the estimate of the cortical current location projected on the surface of brain, separately for nontarget and target stimuli. Both stimuli evoke precentral responses, but for subject 2 the source for targets is 2 cm anterolaterally to the source for nontargets. For subject 7, the difference between the locations is ~1 cm. Figure 8B shows that both attended and nonattended stimuli evoke responses between 145 and 170 ms for subject 2 and between 110 and 140 ms for subject 7. For subject 2, the target ROI captures a signal also between 190 and 240 ms.



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Fig. 8. A: right precentral activity from the visuospatial control experiment is projected on the surface of individual MR images. Areas for Targets and Nontargets are matched to make comparisons between target locations easier. B: amplitude as a function of time for the target and nontarget stimuli. Gray areas mark the same time intervals as in Fig. 7.

In the main experiment, the proportion of epochs containing overt horizontal eye movements was equal during all experimental conditions. After the left hemifield stimuli, horizontal eye movements were detected in 2% of trial, 2% of intertrial, and 3% of passive viewing epochs. After right hemifield stimuli, the corresponding numbers were 1, 3, and 2%.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The results show that focusing attention to a fixation point enhances responses to nonattended peripheral stimuli in the right precentral cortex. The estimated location of the precentral source, between central sulcus and precentral gyrus, corresponds to the known location of human frontal eye field (Paus 1996) (Table 2). Activity of this area has been detected in imaging studies of visuospatial attention (Kim et al. 1999; Nobre et al. 1997; Vandenberghe et al. 1997) and during saccades (Anderson et al. 1994; Sweeney et al. 1996). Its direct stimulation evokes eye movements (Godoy et al. 1990), and patients with cerebral lesions in this area have defects in eye movements (Rivaud et al. 1994). Corbetta (1998) has shown that visuospatial attention and eye movements activate at least partially overlapping cortical areas. Our control studies support the view that visually evoked right FEF responses depend on visual attention. During auditory attention the right FEF was rather silent, making motor preparation and general alertness unlikely causes of its activation. When the visual stimuli were targets, as in the second control study, they also evoked activation with the same latency but perhaps somewhat anterior and lateral to nontarget responses. Our results contrast results of a positron emission tomography study (Corbetta et al. 1993) that found frontal signals close to FEF only to stimuli that were targets for an overt response. The precence of nontarget activation in our study may be due to a different paradigm but also the fact that MEG is especially sensitive to transient changes in the neural activation. On the other hand, Steinmetz et al. (1994), whose paradigm we followed in the visuospatial control experiment, found in monkeys strongest IPL responses to nontarget stimuli. The increased sensitivity in the frontal or parietal areas might also reflect different requirements for the gaze control system during the different experimental conditions. However, all conditions contained a similar small number of overt horizontal saccades giving no support for a simple increased inhibition-of-movement explanation.


                              
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Table 2. Comparison of source locations in Talairach coordinates to studies where visual attention has been directed to peripheral visual field

In conclusion, our findings suggest that the right FEF in humans may be part of a system that during visual attention automatically becomes sensitive to stimuli in all parts of the visual field. Functionally, this might reflect scanning for new stimuli for redirection of attention or eyes, a role Mountcastle et al. (1981, 1987) suggested for the posterior parietal area 7a/PG in monkeys. Monkey data support the scanning function of the FEF. Firing rate in FEF neurons predicts the overt response to a peripheral visual stimulus (Thompson and Schall 1999), and its lesions result in neglect of the contralateral hemispace (Rizzolatti et al. 1983; van der Steen et al. 1986). In humans, right-hemisphere frontal cortex is important for attention to novel stimuli. Its lesions may cause contralateral neglect (Heilman and Valenstein 1972; Maeshima et al. 1994) and prolonged attentional blink (Husain et al. 1997).

The stimulus in this study was not optimal for a detailed study of primary visual areas, but earlier neuromagnetic studies have shown peak V1/V2 activation for luminance and pattern stimuli ~60-90 ms after stimulus onset (Portin et al. 1998, 1999). Although this study concentrated in the early FEF activations (100-160 ms), the same area was active also later. Previously, Nishitani et al. (1999) have found neuromagnetic FEF activation around 290 ms during an eye-finger pursuit task. The beginning of our attention-sensitive FEF activation at 100 ms is in line with monkey data showing that FEF and other dorsal stream responses emerge relatively early during cortical activation (Schmolesky et al. 1998). Rafal and Robertson (1995) suggested that the FEF participates mainly in generation of voluntary saccades and actually inhibits the superior colliculus, which primarily guides the reflexive saccades.

We believe that the functional area producing the IPL responses in this study is the human homologue to monkey 7a. The human IPL, Brodman areas 39 and 40, corresponds most likely to monkey IPL, areas 7a and 7b, also named PG and PF (Grafton et al. 1996; Hyvärinen 1982). In previous human visuospatial attention studies, areas presumably homological to monkey 7a and LIP were active (Corbetta 1998; Nobre et al. 1997). In monkeys 7a is lateral to LIP (Felleman and Van Essen 1991), as is our IPL source compared with some of the earlier imaging data (Table 2). In our study, seven of eight subjects showing right IPL responses displayed activation to both left and right visual field stimuli. Whereas some monkey 7a cells respond to both contra- and ipsilateral visual fields, the LIP cells respond only to contralateral stimuli (Andersen et al. 1990; Blatt et al. 1990; Motter and Mountcastle 1981).

The LIP has more hierarchical ascending connections to FEF (Andersen et al. 1990; Bullier et al. 1996; Felleman and Van Essen 1991) and responds earlier to visual stimuli than the 7a (Barash et al. 1991). Therefore LIP responses in our data should have preceded the FEF responses, whereas we found IPL activity after FEF. In conclusion, both the anatomic location inferior to the intraparietal sulcus and the functional properties of our right IPL signals correspond more to monkey 7a than LIP.

Our individual data show more right than left parietal responses to stimuli in peripheral vision. This is in line with earlier imaging (Corbetta et al. 1993; Kim et al. 1999) and patient studies (Posner et al. 1984; Rafal and Robertson 1995) that show lateralization of parietal activity during redirection of attention. Similarly, saccade latencies for external cues are prolonged more after right than left angular gyrus lesions (Pierrot-Deseilligny et al. 1991).

In monkeys, focused visual attention enhances responses in 7a neurons whose receptive fields are at the nonattended parts of the visual field (Mountcastle et al. 1981, 1987; Steinmetz et al. 1994). However, in our data different individuals showed differences in their response patterns. A lack or weakness of preceding right precentral responses seemed to be a prerequisite for the right IPL sensitivity during visual attention. Perhaps in humans novel peripheral stimuli during focused attention can alternatively be monitored by the right FEF or the right IPL, the latter showing activation with longer latencies. Behavioral data supported this assumption: attention to fixation tended to increase saccade latencies more in subjects who showed the enhancements during focused attention in their IPL area. Accordingly, Pierrot-Deseilligny et al. (1986) have suggested that both the IPL and the FEF can control visually guided saccades. Although individual division of labor between the right IPL and FEF cannot be established by the present data only, this suggestion provides a testable hypothesis for future research.


    ACKNOWLEDGMENTS

We thank R. Hari, S. Salenius, and T. Tanskanen for valuable comments on the manuscript. The MRIs were obtained at the Department of Radiology, Helsinki University Central Hospital.

This study was supported by the Academy of Finland and the Ministry of Education.


    FOOTNOTES

Address for reprint requests: S. Vanni, Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, PO Box 2200, FIN-02015 Espoo, Finland.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 9 July 1999; accepted in final form 5 January 2000.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

0022-3077/00 $5.00 Copyright © 2000 The American Physiological Society