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Cerebral Activity Related to Guessing and Attention During A Visual Detection Task
ABSTRACT CEREBRAL ACTIVITY RELATED TO GUESSING AND ATTENTION DURING A VISUAL DETECTION TASK Paul Azzopardi and Alan Cowey (Department of Experimental Psychology, University of Oxford, Oxford, U.K.)
INTRODUCTION Crick and Koch (1995) have suggested that visual awareness must depend on neural activity in the prefrontal cortex (PFC). This was supported by a functional MRI study of a hemianopic patient with blindsight (subject GY) whose right prefrontal cortex was activated under conditions (i.e. particular values of stimulus parameters) in which he was aware of targets that he could detect in his visual field defect, but not under conditions in which he could detect targets but was not aware of them (Weiskrantz et al., 1995; Sahraie et al., 1997). However, the latter experiment did not assess guessing during the scan itself, despite the fact that guessing might account for the difference in percent correct scores of awareness between the ‘aware’ and ‘unaware’ conditions by reducing response bias in the ‘aware’ condition relative to ‘unaware’ condition, and hence also for the selective activation of the right prefrontal cortex in the ‘aware’ condition (Azzopardi and Cowey, 1998). The present experiment therefore tested the hypothesis that activity in right prefrontal cortex could be related to guessing during visual detection as opposed to visual awareness per se. Guessing is a strategy usually used when stimuli are difficult to detect, necessitating the use of very weak stimuli in this experiment. fMRI studies typically measure brain activity in relation to ceiling levels of behavioural performance using suprathreshold stimuli, so we were also interested to see whether it was possible to measure activation related to the presentation of near-threshold stimuli. In order to maximize sensitivity, an event-related analysis was used. MATERIALS
AND
METHODS
Six normal subjects (3 male, 3 female) detected briefly presented targets under two conditions distinguished only by the instructions given: yes-no (yn), say “yes” if a target was presented, otherwise say “no”; and yes-guess (yg), say “yes” if a target was presented, otherwise guess “yes” or “no”. The targets were vertically oriented, square-wave gratings, 0.5 cpd, 6° x 6°, presented for 250 ms at 6° eccentricity on the horizontal meridian of the right visual field, viewed through the right eye. Three contrasts were used, bracketing each subject’s individual 75% correct threshold as determined in the scanner by a temporal 2-alternative forced-choice adaptive procedure (PEST: Taylor and Creelman, 1967). Blocks of 18 contiguous trials, 9 blanks and 9 targets (3 at each contrast), were presented in randomized order. Each trial consisted of a 100 ms warning tone, followed 250 ms later by a target or blank, followed 1500 ms later by a tone to signify that a response Cortex, (2002) 38, 833-836
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should be made via a button box. The inter-trial interval was 18s. The subject was asked to maintain fixation throughout the entire block, which lasted about 6 minutes. Each subject was given 8 blocks of trials in a single session, 4 blocks per condition in alternation, always starting with the yes-no condition. Blood-oxygen level dependent (BOLD) activation was sampled continuously throughout each block of trials using multislice T2*- weighted gradient echo planar imaging with a TR of 1.5s (3.0s in the case of subject PA) and a flip angle of 70° in a Siemens/Varian 3.0T MRI scanner (fMRIB, Department of Clinical Neurology, University of Oxford). The sampling array consisted of 10 contiguous slices, 64 pixels x 64 pixels in size and 8 mm apart (giving a voxel dimension of 5 × 5 × 8 mm3), inclined so as to cover most of the cortex, including the occipital lobe and the prefrontal cortex. The echoplanar image (EPI) data were concatenated, realigned, spatially smoothed using a 5 × 5 × 5 mm gaussian kernel, and intensity normalized. Data from PA were temporally filtered using a matched bandpass filter (sigma = 2.8, cutoff period 210 s); all other data were corrected by calculating for each time point the difference from baseline (taken as the last TR of the previous trial). After preprocessing, the EPI data were sorted into blocks according to instruction (yes-no or yes-guess), target contrast (3 levels) and outcome (hits, misses, false alarms and correct rejections), and analyzed using ANOVA with timepoints as a treatment and trial as replicates. The resultant Z-scores were then thresholded (Z >= 2.33) to delineate regions of interest.
RESULTS Five cortical regions were designated as regions of interest a priori: left striate cortex (V1), left and right prefrontal cortex, and left and right frontal operculum (FOP). With the exception of left frontal operculum, all of these regions were consistently activated during detection trials. Transient BOLD activation in striate cortex associated with the presentation of targets was found in 5 of the 6 subjects. An example is shown in Figure 1 a. In 3 subjects, the amount of activation mirrored closely both target contrast and behavioural sensitivity (d’), as illustrated in Figure 1 b. Transient activation was found in striate cortex even during blank trials as if a target had been presented, suggesting that it was related to the expectation of a stimulus. Transient activation related to guessing was shown by comparing correct rejection trials in the yes-no and yes-guess conditions. (According to the instructions given in the latter task, a ‘no’ response could have arisen only from a guess, whereas a ‘yes’ response could have arisen from the correct or incorrect detection of a target or from a guess.) Significant increases in signal associated with guessing were found in right prefrontal cortex and right frontal operculum, but not in the left prefrontal cortex (Figure 1c, d). DISCUSSION Visual targets presented briefly at near-threshold contrasts induced consistent, transient increases in BOLD activation in the corresponding part of the striate cortex measured with an event-related paradigm. In general, the percentage change in signal was proportional to the contrast of the target, and hence to its detectability, with two caveats. First, in one case there was no discernable signal
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Fig. 1 – Cerebral BOLD activation related to guessing during a visual detection task. (a) Activation in striate cortex (V1) in the yes-no detection task during target present (12 trials per contrast: o = 0.45%, . = 0.6%, ∇ = 0.9%; j = mean) and target absent (•; n = 36) trials, recorded from subject PA. (b) Stimulus-related activation in V1 compared with stimulus detectability (d’) in the yes-no detection task for subject PA. (c) Guessing related activation in right prefrontal cortex of subject PA revealed by the difference in BOLD signal measured during correct-rejection trials in the yes-no and yes-guess conditions. Guessing is indicated by the increase in false alarm rate (F) in the yes-guess task (F = 0.222) relative to the yes-no task (F = 0.000). (d) Activation related to guessing in frontal regions of interest (ROIs) averaged across 6 subjects (Key: rFOP = right frontal operculum; rPFC = right prefrontal cortex; lPFC = left prefrontal cortex. Bars indicate 95% confidence limits).
in striate cortex associated with the presence of a target despite the fact the subject could detect the stimuli as well as any other subject. Secondly, in every case in which a transient BOLD signal was associated with presence of a target, a transient signal with a similar time-course was also detected during blank trials, as if related to the expectation of a target. This provides direct evidence for attentional modulation of activity in primary visual cortex. A practical implication of these findings is that, with barely-detectable targets, neither the presence nor the absence of a BOLD signal gives a completely reliable indication of the cortical response to the target. The results of the experiment show that guessing can activate regions of the right frontal cortex whose activity has previously been thought to indicate
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awareness. Guessing can be an effective of way of reducing a subject’s response bias (i.e. his tendency to say “yes” independently of whether or not a stimulus was presented). By doing so it is capable of producing an apparent dissociation (measured in percentage correct score) between performance (assessed by ‘forced guessing’) and awareness (assessed by a ‘yes-no’ task) in visual detection, as is sometimes found in hemianopic subjects (Azzopardi and Cowey, 1998). Therefore the possibility of guessing must be controlled for explicitly by comparing false alarm rates in the ‘aware’ and ‘unaware’ conditions before concluding that a dissociation exists between performance and awareness. In the presence of guessing (indicated by a relatively high false alarm rate), it would be unsafe to attribute BOLD activation in the right frontal cortex to processes mediating visual awareness without further controls. Acknowledgements. This work was supported by the Medical Research Council, Grant No. G971/387/B. The authors are grateful for advice or technical assistance from Caroline Andrews, Stuart Clare, David Flitney, Peter Hobden, David Homfray, Peter Jezzard, Arthur Magill, Paul Matthews, Stephen Smith and Irene Tracey (fMRIB, Dept. of Clinical Neurology, Oxford), and Morten Kringelbach and Stephen Young (Dept. of Experimental Psychology, Oxford). REFERENCES AZZOPARDI P and COWEY A. Blindsight and visual awareness. Consciousness and Cognition, 7: 292-311, 1998. CRICK F and KOCH C. Are we aware of neural activity in primary visual cortex? Nature, 375: 121-123, 1995. SAHRAIE A, WEISKRANTZ L, BARBUR JL, SIMMONS A, WILLIAMS SC and BRAMMER MJ. Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. Proceedings of the National Academy of Sciences U.S.A., 94: 9406-11, 1997. TAYLOR MM and CREELMAN CD. PEST: Efficient estimates on probability functions. Journal of the Acoustical Society of America, 46: 782-787, 1967. WEISKRANTZ L, BARBUR JL and SAHRAIE A. Parameters affecting conscious versus unconscious visual discrimination with damage to the visual cortex (V1). Proceedings of the National Academy of Sciences U.S.A., 92: 6122-6, 1995. Paul Azzopardi, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, U.K. e-mail: [email protected]
INTRODUCTION Crick and Koch (1995) have suggested that visual awareness must depend on neural activity in the prefrontal cortex (PFC). This was supported by a functional MRI study of a hemianopic patient with blindsight (subject GY) whose right prefrontal cortex was activated under conditions (i.e. particular values of stimulus parameters) in which he was aware of targets that he could detect in his visual field defect, but not under conditions in which he could detect targets but was not aware of them (Weiskrantz et al., 1995; Sahraie et al., 1997). However, the latter experiment did not assess guessing during the scan itself, despite the fact that guessing might account for the difference in percent correct scores of awareness between the ‘aware’ and ‘unaware’ conditions by reducing response bias in the ‘aware’ condition relative to ‘unaware’ condition, and hence also for the selective activation of the right prefrontal cortex in the ‘aware’ condition (Azzopardi and Cowey, 1998). The present experiment therefore tested the hypothesis that activity in right prefrontal cortex could be related to guessing during visual detection as opposed to visual awareness per se. Guessing is a strategy usually used when stimuli are difficult to detect, necessitating the use of very weak stimuli in this experiment. fMRI studies typically measure brain activity in relation to ceiling levels of behavioural performance using suprathreshold stimuli, so we were also interested to see whether it was possible to measure activation related to the presentation of near-threshold stimuli. In order to maximize sensitivity, an event-related analysis was used. MATERIALS
AND
METHODS
Six normal subjects (3 male, 3 female) detected briefly presented targets under two conditions distinguished only by the instructions given: yes-no (yn), say “yes” if a target was presented, otherwise say “no”; and yes-guess (yg), say “yes” if a target was presented, otherwise guess “yes” or “no”. The targets were vertically oriented, square-wave gratings, 0.5 cpd, 6° x 6°, presented for 250 ms at 6° eccentricity on the horizontal meridian of the right visual field, viewed through the right eye. Three contrasts were used, bracketing each subject’s individual 75% correct threshold as determined in the scanner by a temporal 2-alternative forced-choice adaptive procedure (PEST: Taylor and Creelman, 1967). Blocks of 18 contiguous trials, 9 blanks and 9 targets (3 at each contrast), were presented in randomized order. Each trial consisted of a 100 ms warning tone, followed 250 ms later by a target or blank, followed 1500 ms later by a tone to signify that a response Cortex, (2002) 38, 833-836
834
Paul Azzopardi and Alan Cowey
should be made via a button box. The inter-trial interval was 18s. The subject was asked to maintain fixation throughout the entire block, which lasted about 6 minutes. Each subject was given 8 blocks of trials in a single session, 4 blocks per condition in alternation, always starting with the yes-no condition. Blood-oxygen level dependent (BOLD) activation was sampled continuously throughout each block of trials using multislice T2*- weighted gradient echo planar imaging with a TR of 1.5s (3.0s in the case of subject PA) and a flip angle of 70° in a Siemens/Varian 3.0T MRI scanner (fMRIB, Department of Clinical Neurology, University of Oxford). The sampling array consisted of 10 contiguous slices, 64 pixels x 64 pixels in size and 8 mm apart (giving a voxel dimension of 5 × 5 × 8 mm3), inclined so as to cover most of the cortex, including the occipital lobe and the prefrontal cortex. The echoplanar image (EPI) data were concatenated, realigned, spatially smoothed using a 5 × 5 × 5 mm gaussian kernel, and intensity normalized. Data from PA were temporally filtered using a matched bandpass filter (sigma = 2.8, cutoff period 210 s); all other data were corrected by calculating for each time point the difference from baseline (taken as the last TR of the previous trial). After preprocessing, the EPI data were sorted into blocks according to instruction (yes-no or yes-guess), target contrast (3 levels) and outcome (hits, misses, false alarms and correct rejections), and analyzed using ANOVA with timepoints as a treatment and trial as replicates. The resultant Z-scores were then thresholded (Z >= 2.33) to delineate regions of interest.
RESULTS Five cortical regions were designated as regions of interest a priori: left striate cortex (V1), left and right prefrontal cortex, and left and right frontal operculum (FOP). With the exception of left frontal operculum, all of these regions were consistently activated during detection trials. Transient BOLD activation in striate cortex associated with the presentation of targets was found in 5 of the 6 subjects. An example is shown in Figure 1 a. In 3 subjects, the amount of activation mirrored closely both target contrast and behavioural sensitivity (d’), as illustrated in Figure 1 b. Transient activation was found in striate cortex even during blank trials as if a target had been presented, suggesting that it was related to the expectation of a stimulus. Transient activation related to guessing was shown by comparing correct rejection trials in the yes-no and yes-guess conditions. (According to the instructions given in the latter task, a ‘no’ response could have arisen only from a guess, whereas a ‘yes’ response could have arisen from the correct or incorrect detection of a target or from a guess.) Significant increases in signal associated with guessing were found in right prefrontal cortex and right frontal operculum, but not in the left prefrontal cortex (Figure 1c, d). DISCUSSION Visual targets presented briefly at near-threshold contrasts induced consistent, transient increases in BOLD activation in the corresponding part of the striate cortex measured with an event-related paradigm. In general, the percentage change in signal was proportional to the contrast of the target, and hence to its detectability, with two caveats. First, in one case there was no discernable signal
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Fig. 1 – Cerebral BOLD activation related to guessing during a visual detection task. (a) Activation in striate cortex (V1) in the yes-no detection task during target present (12 trials per contrast: o = 0.45%, . = 0.6%, ∇ = 0.9%; j = mean) and target absent (•; n = 36) trials, recorded from subject PA. (b) Stimulus-related activation in V1 compared with stimulus detectability (d’) in the yes-no detection task for subject PA. (c) Guessing related activation in right prefrontal cortex of subject PA revealed by the difference in BOLD signal measured during correct-rejection trials in the yes-no and yes-guess conditions. Guessing is indicated by the increase in false alarm rate (F) in the yes-guess task (F = 0.222) relative to the yes-no task (F = 0.000). (d) Activation related to guessing in frontal regions of interest (ROIs) averaged across 6 subjects (Key: rFOP = right frontal operculum; rPFC = right prefrontal cortex; lPFC = left prefrontal cortex. Bars indicate 95% confidence limits).
in striate cortex associated with the presence of a target despite the fact the subject could detect the stimuli as well as any other subject. Secondly, in every case in which a transient BOLD signal was associated with presence of a target, a transient signal with a similar time-course was also detected during blank trials, as if related to the expectation of a target. This provides direct evidence for attentional modulation of activity in primary visual cortex. A practical implication of these findings is that, with barely-detectable targets, neither the presence nor the absence of a BOLD signal gives a completely reliable indication of the cortical response to the target. The results of the experiment show that guessing can activate regions of the right frontal cortex whose activity has previously been thought to indicate
836
Paul Azzopardi and Alan Cowey
awareness. Guessing can be an effective of way of reducing a subject’s response bias (i.e. his tendency to say “yes” independently of whether or not a stimulus was presented). By doing so it is capable of producing an apparent dissociation (measured in percentage correct score) between performance (assessed by ‘forced guessing’) and awareness (assessed by a ‘yes-no’ task) in visual detection, as is sometimes found in hemianopic subjects (Azzopardi and Cowey, 1998). Therefore the possibility of guessing must be controlled for explicitly by comparing false alarm rates in the ‘aware’ and ‘unaware’ conditions before concluding that a dissociation exists between performance and awareness. In the presence of guessing (indicated by a relatively high false alarm rate), it would be unsafe to attribute BOLD activation in the right frontal cortex to processes mediating visual awareness without further controls. Acknowledgements. This work was supported by the Medical Research Council, Grant No. G971/387/B. The authors are grateful for advice or technical assistance from Caroline Andrews, Stuart Clare, David Flitney, Peter Hobden, David Homfray, Peter Jezzard, Arthur Magill, Paul Matthews, Stephen Smith and Irene Tracey (fMRIB, Dept. of Clinical Neurology, Oxford), and Morten Kringelbach and Stephen Young (Dept. of Experimental Psychology, Oxford). REFERENCES AZZOPARDI P and COWEY A. Blindsight and visual awareness. Consciousness and Cognition, 7: 292-311, 1998. CRICK F and KOCH C. Are we aware of neural activity in primary visual cortex? Nature, 375: 121-123, 1995. SAHRAIE A, WEISKRANTZ L, BARBUR JL, SIMMONS A, WILLIAMS SC and BRAMMER MJ. Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. Proceedings of the National Academy of Sciences U.S.A., 94: 9406-11, 1997. TAYLOR MM and CREELMAN CD. PEST: Efficient estimates on probability functions. Journal of the Acoustical Society of America, 46: 782-787, 1967. WEISKRANTZ L, BARBUR JL and SAHRAIE A. Parameters affecting conscious versus unconscious visual discrimination with damage to the visual cortex (V1). Proceedings of the National Academy of Sciences U.S.A., 92: 6122-6, 1995. Paul Azzopardi, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, U.K. e-mail: [email protected]