7 1 Relating single cell studies and population measures
7.3 What is the relationship between attention and visual awareness?
The relationship between attention and awareness has been of enduring interest, although the exact nature o f the connection rem ains elusive. O ur observation that the degree to w hich unattended stimuli are processed depends on the level of perceptual load raises the possibility that allocation o f attention is necessary (though not sufficient) for visual awareness. In section 5.1.1. , an ignored visual motion stimulus does not produce activity in cortical area V 5 /M T under conditions o f high perceptual load. This study did not directly address w hether subjects were aware of the stimulus (by, for example, debriefing them ) but nevertheless, given the absence of activity in V5 under high load it is difficult to see how perception would not be altered. Evidence from other studies dem onstrates the im portance of activity in V5 com plex for awareness o f visual motion. Activity in V5 is associated with awareness o f a m oving grating during binocular rivalry and is abolished w h e n the grating is not seen (L um er et a i , 1998; L u m e r and Rees, 1999). S im ilarly, lesions to V5 give rise to an inability to be aware of visual motion. On the basis o f these and other findings, it has been proposed that conscious aw areness of visual m otion is c au se d by activity in V5 (though we have argued elsewhere that an interaction between d ifferent cortical areas is necessary). So were our subjects aware o f the visual motion stim ulus under conditions o f high perceptual load?
A clearer answer to the issue is provided by the experiment presented in C hapter 6 . Here we provide an explicit m easure of awareness by asking subjects w hether they are able to rem e m b e r attended and unattended stimuli. Even when foveally presented, subjects are unable to recall the identity o f single words when unattended. T he brain activity evoked by the un a tte n d ed w ords is no different to that evoked by m eaningless stim uli. This ^ th ere fo re provides inform ation about how a particular aspect o f word processing, the extraction o f meaning, is affected by the absence o f attention. W hile it is difficult to draw strong conclusions from a null result, our findings strongly suggest that under conditions o f full inattention, the brain does not extract sem antic inform ation from u n a tte n d ed
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stim uli. M oreover, subjects appeared unaw are o f the presence o f such stim uli, show ing in a tten tio n al blin dn ess. T his suggests not only that attentio n is im p o rtan t fo r the extraction o f m eaning from stim uli, but also that this extraction o f identity is in som e sense im portant for stimuli to reach awareness.
T aken together, the experim ents in C hapter 5 & C hap ter 6 suggest that w hether un atten ded visual stim uli are processed depends on the perceptual load o f the prim ary task th a t su bjects are engaged in. T he effectiv e locus o f selection (in inform ation p ro cessin g term s) varies accordingly. W ith a very sim ple task (C hapter 4 ) and co rrespo nd in gly low perceptual load, stim ulus processing proceeds to extraction of categorical identity o f ignored stimuli. As a result, negative prim ing occurs and activity is seen in su b co rtical structu res such as the corpus striatum . A s p ercep tu al load is system atically increased, activity in a distributed network of cortical areas associated with processin g an ignored stim ulus is reduced. W hen load is sufficiently high un der very dem anding task conditions, unattended stim uli are no longer rem em bered. U nder these conditions the locus o f selection appears to be at, or prior to, the extraction o f m eaning. U nattend ed stim uli are sim ply not perceived. These findings do not establish w hether unattended stim uli fail to be perceived under all circum stances (e.g. (Treism an, I960)), but do dem onstrate clearly that circum stances exist under w hich no perception occurs.
Is this true for all classes o f stim uli? E arlier w ork has em phasised that un der certain conditions, unattended stim ulus processing may occur. H ow ever in such experim ents it has not been feasible to exclude the possibility that some attention was available, leading to p ro cessing o f unattended stim uli. In other w ords, the issue is how to ensure in a rigorous and quantitative m anner that attention is truly unavailable w hen m easuring the p ro cessing o f unattended stim uli. The present findings im ply that unattended stim ulus processing w ill occur autom atically if attention is available. H ow ever, it rem ains unclear w hether the processing of certain stim uli requires so little attention that a stim ulus can be detected even w hen attention is allocated elsew here in the visual field. These issues have been addressed in a series o f experim ents by Braun & colleagues (Braun, 1993; Braun and Ju lesz, 1998; B raun and Sagi, 1991). B raun has used an asym m etrical dual task e x p e rim e n t w h ere atten tio n is fo c u se d on a p rim ary le tte r task th a t in v o lv es discrim inating five random ly rotated letters (Ts or Ls) near the centre of the display. This task is particularly dem anding, leaving little or no attention available for central tasks. T his can be establish ed by producing an attention o peratin g characteristic (directly
V~
N eural correlates of selective attention
analogous to a receiver operating characteristic) when perform ing this central letter task w ith a particular secondary probe task (identification o f a single letter). The authors then com bined the central letter task with a num ber of peripheral tasks, including detection of a texture pop-out stim uli. The results show that a num ber o f peripheral pop out tasks can be perfo rm ed concu rren tly w ith the central letter task w ith little or no dual task interference. This strongly suggests that certain types o f visual processing leading to aw areness are possible w ithout attention. The detection o f pop out targets preattentively has also been investigated by presented subjects w ith a task requiring detection o f a pop out during the ‘attentional b lin k ’. Joseph and colleagues (Joseph et a l , 1997) found that subjects w ere unable to detect such popouts during concurrent detection o f a single target letter in a rapid serial stream. H ow ever it appears that this pattern of results is only seen w ith naive subjects, as repeated training leads to subjects being able to perform both tasks w ith ease (Braun, 1998). This sensitivity to training is not seen in the w ork of B raun and colleagues, who invariably use highly overtrained observers.
In sum m ary, while higher level properties o f visual stim uli appear to receive very little processing w ithout attention, there is some evidence to suggest preattentive processing of pop-out visual stimuli. These results with asymm etric dual task paradigm s are com patible w ith the present findings if attention is only required for processing certain classes of stim uli (such as the words investigated in Chapter 6 ) or for certain processing stages (such as the extraction of m eaning). The results o f B raun and colleagues suggest that certain classes of visual stim uli are privileged in the sense that the detection o f such stim uli does not require attention. It will be o f considerable interest to see how these psychophysical findings are reflected in future brain im aging studies.
7.4 Conclusion
T his thesis has described a num ber o f experim ents th at share a com m on them e o f in v e stig a tin g the n atu re and ex ten t o f u n a tte n d e d s tim u lu s p re se n ta tio n . T h e psychological concept of resource lim itation has em erged as an im portant determ inant o f u n atten d ed processing, although its anatom ical em b o d im en t is unclear. T h e w ork p resented here has attem pted to start building som e links betw een relatively abstract c o g n itiv e theories o f attention, functional im aging w ork in hum ans and sin gle cell electrophysiology in aw ake behaving prim ates. F uture w ork should seek to clarify the nature o f resource constraints in anatom ical and p hy siological term s. A m echanistic
N eural correlates of selective attention
account of attention in terms o f interacting structures and processes in the brain is highly desirable. To approach such an undertaking requires a synthesis o f phenom enology, psychophysics and physiology in order to provide a description of the nature and extent o f visual attention and its relationship to visual awareness.
Neural correlates of selective attention