Consciousness absent and present: a neurophysiological exploration

13 Pages·2004·0.64 MB·English

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ProgressinBrainResearch,Vol.144
ISSN0079-6123
(cid:1)2004ElsevierBV.Allrightsreserved
CHAPTER 6
Consciousness absent and present:
a neurophysiological exploration
Edmund T. Rolls*
UniversityofOxford,DepartmentofExperimentalPsychology,OxfordOX13UD,UK
Abstract: Backward masking was used to investigate the amount of neuronal activity that occurs in the macaque
inferior temporal visual cortex when faces can just be identified. It is shown that the effect of the pattern mask is to
interrupt neuronal activity in the inferior temporal visual cortex. This reduces the number of action potentials that
occurtoagivenstimulus,anddecreasesevenmoretheinformationthatisavailableaboutwhichstimuluswasshown
becausethevarianceofthespikecountsisincreased.Whentheonsetofthemaskfollowstheonsetoftheteststimulus
by 20 ms, each neuron fires for approximately 30 ms, provides on average 0.06 bits of information, and human
observers perform at approximately 50% better than chance in forced choice psychophysics, yet say that they are
guessing,andfrequentlyreportthattheyareunabletoconsciouslyseethefaceandidentifywhichfaceitis.Atalonger
StimulusOnsetAsynchronyof40ms,theneuronsfireforapproximately50ms,theamountofinformationcarriedbya
singleneuronis0.14bits,andhumanobserversaremuchmorelikelytoreportconsciousidentificationofwhichface
was shown. The results quantify the amount of neuronal firing and information that is present when stimuli can be
discriminated but not reported on consciously, and the additional amount of neuronal firing and information that is
requiredforhumansobserverstoconsciouslyidentifythefaces.Itissuggestedthatthethresholdforconsciousvisual
perceptionmaybesettobehigherthanthelevelatwhichsmallbutsignificantinformationispresentinneuronalfiring,
sothatthesystemsinthebrainthatimplementthetypeofinformationprocessinginvolvedinconsciousthoughtsare
notinterrupted bysmallsignals thatcould benoisein sensory pathways.
Introduction visual perception of the test visual stimulus, and this
paradigm has been widely used in psychophysics
Damage to the primary (striate) visual cortex can (Humphreys and Bruce, 1989). In this chapter the
resultinblindsight,inwhichpatientsreportthatthey authorconsidershowmuchinformationispresentin
do not see stimuli consciously, yet when making neuronal firing in the part of the visual system that
forced choices can discriminate some properties of represents faces and objects, the inferior temporal
thestimulisuchasmotion,position,someaspectsof visual cortex (Rolls and Deco, 2002), when human
form, and even face expression (Weiskrantz et al., subjectscandiscriminateinforcedchoice,butcannot
1974; Stoerig and Cowey, 1997; Weiskrantz, 1997, consciously perceive, face identity. The author also
1998; De Gelder et al., 1999). In normal human considers the implications that the neurophysiologi-
subjects, backward masking of visual stimuli, in cal findings have for consciousness.
which another visual stimulus closely follows the The representation of faces and objects is in
short presentation of a test stimulus, reduces the the inferior temporal visual cortex as shown by
evidence that position, size and even for some
neurons view, invariant representations of objects
*Correspondingauthor.Tel.: þ44-1865-271348;
and faces are provided by neurons in the inferior
Fax: þ44-1865-310447;Web:www.cns.ox.ac.uk;
E-mail:[email protected] temporal visual cortex (Rolls, 2000a; Rolls and
DOI:10.1016/S0079-6123(03)14400-6 95
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Deco, 2002); that this is the last stage of unimodal visual cortex and perceptual studies in humans
visual processing in primates; and that lesions of with the paradigm of backward masking of visual
what may be a homologous region in humans, stimuli (Rolls et al., 1994, 1999; Rolls and Tove´e,
the fusiform gyrus face and object areas (Ishai 1994). A subsequent study by Kovacs et al. (1995)
et al., 1999; Kanwisher et al., 1997), produce face using a similar backward masking paradigm
and object identification deficits in the absence of combined with primate electrophysiology confirmed
low-level impairments of visual processing such as the results.
visual acuity (Rolls and Deco, 2002; Farah, 1990;
Farah et al., 1995a,b). The inferior temporal visual
cortex is, therefore, an appropriate stage of Neurophysiology of the backward masking of
processing at which to relate quantitative aspects visual stimuli
of neuronal processing to the visual perception of
faces and objects. We have, therefore, studied the Rolls and Tove´e (1994) and Rolls et al. (1994)
quantitative relationship between neuronal activity measured the responses of single neurons in the
in the macaque inferior temporal visual cortex and macaque inferior temporal visual cortex during
visual perception (Rolls and Deco, 2002), and in backward visual masking. Neurons that were
this article the focus is on the relation between selective for faces, using distributed encoding (Rolls
inferior temporal visual cortex and conscious and Tove´e, 1995; Rolls et al., 1997; Treves et al.,
visual perception, using the results from combined 1999; Rolls and Deco, 2002), were tested in a visual
neurophysiological studies on the inferior temporal fixation task run as shown in Fig. 1. The visual
Tone
Fixation spot
Visual
stimulus
S.O.A.
Mask
Firing rate
measurement
-500 0 500 1000 1500 2000
Time (ms)
Fig. 1. The timing used in the backward masking visual fixation blink task. The Stimulus Onset Asynchrony is the time between
theonsetofthevisualteststimulusandtheonsetofthepatternmaskstimulus.Theteststimulusdurationwas16ms.(AfterRolls
etal.,1994.)
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fixation task was used to ensure that the monkey the test image was present at the start of the next
looked at the visual stimuli. frame. Stimulus Onset Asynchrony (S.O.A.) values
The methods used are described by Rolls and of 20, 40, 60, 100 or 1000 ms (chosen in a random
Tove´e(1994)andRollsetal.(1994),andafewsalient sequence by the computer) were used. (The Stimulus
points follow. As shown in Fig. 1, at (cid:2)100 ms, the Onset Asynchrony is the time between the onset of
fixation spot was blinked off so that there was no the test stimulus and the onset of the mask.) The
stimulus on the screen in the 100 ms period duration of the masking stimulus was 300 ms. The
immediately preceding the test image. The screen in stimuliwerestaticvisualstimulisubtending8degrees
thisperiod,andatallothertimesincludingtheinter- in the visual field presented on a video monitor at a
stimulus interval and the interval between the test distance of 1.0 m. The faces used as test stimuli are
image and the mask, was set at the mean luminance illustrated in Fig. 2. The usual masking stimulus
of the test images and the mask, so that pattern (towhichtheneuronbeinganalyseddidnotrespond)
discrimination with equally intense test and mask was made up of letters of the alphabet {N,O}, as
stimuliwasinvestigated(seeBruceandGreen,1989). shown in Fig. 2. The masking pattern consisted of
At0 ms, the500 mswarning curetone was switched overlapping letters, and this masking pattern was
offandthetestvisualimagewasswitchedonforone used because it is similar to the mask used in the
16 ms frame of a raster display image. The monitor previouspsychophysicalexperiments(seeRollsetal.,
hadapersistenceoflessthan3ms,sothatnopartof 1994).(Insomecasesthemaskingstimuluswasaface
Fig.2. Examplesofthetestimagesused.Themaskisalsoshown.(AfterRollsetal.,1994.)
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stimulus that was ineffective for the neuron being mately 75 ms, and this firing lasted for 200–300 ms,
recorded.) thatisformuchlongerthanthe16mspresentationof
Figure 3 shows examples of the effects of the target stimulus. In the next pairs down, the
backward masking on the responses of a single effects of introducing a non-effective face as the
inferior temporal cortex neuron in peristimulus masking stimulus with different S.O.A.s are shown.
rastergram and time histogram form. The top It is shown that the effect of the mask is to limit
rastergram/spike density histogram pair shows the the duration of the firing produced by the target
responses of the neuron to a single frame of the test stimulus. Very similar masking was obtained with
stimulus (an effective face stimulus for that neuron). thestandardN–Opatternmask.Similarexperiments
Relativetotheprestimulusrate,therewasanincrease wererepeatedon42differentcells(Rollsetal.,1994;
in the firing produced with a latency of approxi- Rolls and Tove´e, 1995), and in all cases the
Fig.3. Peristimulusrastergramsandsmoothedperistimulusspikedensityhistogramsbasedonresponsesin8–16trialstothetestface
alone (top raster-histogram pair), and to the test face followed by a masking stimulus (which was a face that was ineffective in
activatingthecell)withdifferentS.O.A.values.(S.O.A.¼StimulusOnsetAsynchrony)Themaskalonedidnotproducefiringinthe
cell.Thetargetstimuluswasshownfor16msstartingattime0.(Thetoptraceshowstheresponsetothetargetstimulusalone,inthat
withthis1000msS.O.A.,themaskstimuluswasdelayeduntilwellaftertheendoftherecordingperiodshown.)(AfterRollsand
Tove´e,1994.)
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temporalaspectsofthemaskingweresimilartothose responses, averaged across the population of 15
shown in Fig. 3. neurons for which a sufficient number of trials was
One important conclusion from these results is available, is shown in Fig. 4. The responses for the
that the effect of a backward masking stimulus on most (max) and the least (min) effective stimuli are
cortical visual information processing is to limit the shown for the period 0–200 ms with respect to
duration of neuronal responses, by interrupting stimulusonset.Therewaslittleeffect(notsignificant)
neuronal firing. The neuronal firing of inferior tem- of the mask on the responses to the least effective
poral cortex neurons often persisted for 200–300 ms stimulus in the set, for which the number of spikes
aftera16mspresentationofastimulus.Witha20ms was close to the spontaneous activity.
Stimulus Onset Asynchrony, the neuronal firing was The transmitted information carried by neuronal
typically limited to 30 ms. With a 40 ms Stimulus firing rates about the stimuli was computed with the
Onset Asynchrony, the neuronal firing was typically useoftechniquesthathavebeendescribedpreviously
limitedto50ms.Thispersistenceofcorticalneuronal (e.g.,Rollsetal.,1997;RollsandTreves,1998;Rolls
firing when a masking stimulus is not present is and Deco, 2002), and have been used previously
probably related to cortical recurrent collateral to analyse the responses of inferior temporal cortex
connections which could implement an autoassocia- neurons (Optican and Richmond, 1987; Gawne and
tive network with attractor and short-term memory Richmond,1993;Tove´eetal.,1993;Tove´eandRolls,
properties (see Rolls and Treves, 1998; Rolls and 1995; Rolls et al., 1997). In brief, the general
Deco, 2002), because such continuing post-stimulus procedure was as follows (Rolls et al., 1999). The
neuronal firing is not observed in the lateral geni- response r of a neuron to the presentation of a
culatenucleus(K.Martin,personalcommunication). particularstimulusswascomputedbymeasuringthe
firingrateoftheneuroninafixedtimewindowafter
Information available in inferior temporal cortex
visual neurons during backward masking Max.
11 Min.
To fully understand quantitatively the responses of
inferiortemporal cortexneuronsat thethresholdfor
10
visual perception, Rolls et al. (1997) applied
information theoretic methods (see Shannon, 1948;
RollsandTreves,1998;RollsandDeco,2002)tothe 9
analysis of the neurophysiological data with back-
ward masking obtained by Rolls et al. (1994) and ms
adcnRoniuosnamcldllrysbiimsteiiraosinnnoadisfst,esTpbthioybkaveetetts´wea,iketbei(un1nstg9h9aot4ilhwns)eo.tsotOshhtanoeimcewcvuoaaluriwdinavetbulalinnlnidtttoaeyhtgreefrodonnoimefflfyuertrtortehihnnaiesstl mber of spikes in 0 - 200 78
to trial in the number of spikes. Another advantage Nu 6
of this analysis is that it evaluates the extent to
which the neurons discriminate between stimuli in
5
bits, which can then be directly compared with
evidence about discriminability obtained using
different measures, such as human psychophysical 4 20 40 60 100 no mask
performance. The analysis quantifies what can be Stimulus Onset Asynchrony (ms)
determined about which of the set of faces was
Fig.4. Themean((cid:4)sem)acrosscellsofthenumberofspikes
presented from a single trial of neuronal firing.
produced by the most effective stimulus (max) and the least
As a preliminary to the information theoretic
effective stimulus (min) as a function of Stimulus Onset
analysis, the effect of the S.O.A. on the neuronal Asynchrony(S.O.A.).(AfterRollsetal.,1999.)
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the stimulus presentation. The firing rates were then Figure 5 shows the average across the cells of the
quantizedintoasmallernumberofbinsdthanthere cumulated information available in a 200 ms period
were trials for each stimulus. After this response from stimulus onset from the responses of the 15
quantization, the experimental joint stimulus- neurons as a function of the S.O.A. This emphasizes
response probability table P(s,r) was computed how as the S.O.A. is reduced towards 20 ms
from the data (where P(r) and P(s) are the the information does reduce rapidly, but that
experimental probability of occurrence of responses nevertheless at an S.O.A. of 20 ms there is still
and of stimuli respectively), and the information considerable information about which stimulus was
I(S,R) transmitted by the neurons averaged across shown. The reduction of the information at different
the stimuli was calculated by using the Shannon S.O.A.s was highly significant(one way ANOVA) at
formula (Shannon, 1948; Rolls and Deco, 2002): P<0.001. It was notable that the information
reduced much more than the number of spikes on
X Pðs,rÞ each trial as the S.O.A. was shortened. The
IðS,RÞ¼ Pðs,rÞlog
2 PðsÞPðrÞ explanation for this is that at short S.O.A.s the
s,r
neuronalresponsesbecomenoisy,asshownbyRolls
etal.(1999).Thisemphasizesthevalueofmeasuring
andthensubtractingthefinitesamplingcorrectionof
the information available, and not only the number
Panzeri and Treves (1996), to obtain estimates
of spikes (Rolls et al., 1999).
unbiased for the limited sampling. This leads to the
information available in the firing rates about the
stimulus.
Human psychophysical performance with the same
Information in 0 - 200 ms set of stimuli
0.4
Rolls et al. (1994) performed human psychophysical
0.35 experimentswiththesamesetofstimuliandwiththe
same apparatus used for the neurophysiological
experiments so that the neuronal responses could be
0.3 closely related to the identification that was possible
of which face was shown. The monitor provided
maximum and minimum luminance of 6 and 0.13
0.25
mation (bits) 0.2 flionoeFtaliravimteyb,deiwrfftiestrh,einnatanfndaceerswroawrseorfeanduojsuemsdteoadrsestithnimatenurnl3ia%.lAl.yll tfhoer
Infor faces were well known to each of the eight observers
used in the experiment. In the forced choice
0.15
paradigm, the observers specified whether the face
was normal or rearranged, and identified whose face
0.1 they thought had been presented. Even if the
observers were unsure of their judgement they were
instructed to respondwith their best guess. The data
0.05
were corrected for guessing to aid in comparison
betweenclassificationandidentification.Thiscorrec-
0 tion arranged that chance performance would be
20 40 60 100 no mask
Stimulus Onset Asynchrony (ms) shown as 0% correct on the graphs, and perfect
performance as 100% correct.
Fig. 5. The average ((cid:4)sem) across the cells of the cumulated
The mean proportion of correct responses for
information available in a 200 ms periodfromstimulus onset
the identification task (and for the classification of
fromtheresponsesofthecellsasafunctionoftheS.O.A.(After
Rollsetal.,1999.) normal versus rearranged) are shown in Fig. 6. The
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Psychophysical performance on face identification
throughout a trial). Sometimes the subjects had
someconsciousfeelingthatapartofaface(suchasa
1.0
mouth)hadbeenshown. However, thesubjectswere
notconsciousofseeingawholeface,orofseeingthe
faceofaparticularperson.AtanS.O.A.of40ms,the
0.8
subjects’ forced choice performance of face identifi-
cation was close to 100% (see Fig. 6), and at this
orrect0.6 S.O.A., the subjects became much more consciously
n c aware of the identity of which face had been shown
o
porti Face type (Rolls et al., 1994).
Pro0.4
Normal Rearranged
Task
Discussion
0.2 Configuration
Identification The neurophysiological data (Rolls et al., 1994;
Rolls and Tove´e, 1994), and the results of the
0.0
information theoretic analysis (Rolls et al., 1999),
can now be compared directly with the effects of
-0.2 backward masking in human observers, studied in
20 40 60 80 100 120
the same apparatus with the same stimuli (Rolls
Stimulus Onset Asynchrony (ms)
et al., 1994). For the human observers, identification
Fig.6. Psychophysicalperformanceofhumanswiththesame of which face from a set of six had been seen was
stimuliasusedintheneurophysiologicalexperimentsdescribed 50% correct (with 0% correct corresponding to
here.Thesubjectswereshown‘normal’facesorfaceswiththe
chance performance) with an S.O.A. of 20 ms, and
parts‘rearranged’,andwereaskedtostatewhichof5faceshad
97% correct with an S.O.A. of 40 ms (Rolls et al.,
beenshown(‘Identification’),andwhetherthefaceshownwas
inthenormalorrearranged‘Configuration’.Theplotsshowthe 1994). Comparing the human performance purely
proportion correct on the tasks of classification of spatial with the changes in firing rate under the same
configuration (i.e., whether the face features were normal or stimulus conditions suggested that when it is just
rearranged), and of determination of the identity of the faces
possible to identify which face has been seen,
forfacesintheNormalorRearrangedspatialconfigurationof
neurons in a given cortical area may be responding
face features, as a function of Stimulus Onset Asynchrony
(S.O.A).Thedatahavebeencorrectedforguessing.Themeans for only approximately 30 ms (Rolls and Tove´e,
of the proportions correct are shown. The test stimulus was 1994; Rolls et al., 1994). The implication is that
presentedfor16ms.(AfterRollsetal.,1994.) 30 ms is enough time for a neuron to perform
sufficient computation to enable its output to be
used for identification. The results based on an
proportion correct data was submitted to an arc sin analysis of the information encoded in the spike
transformation (to normalise the data) and a trainsatdifferent S.O.A.s supportthishypothesisby
repeated measures ANOVA was performed. This showing that a significant proportion of information
analysis showed statistically significant effects of is available in these few spikes (see Fig. 5), with on
S.O.A. [F(4,28)¼61.52, P<0.0001]. average 0.06 bits available from each neuron at an
Forced choice discrimination of face identity was S.O.A. of 20 ms. Thus when subjects feel that they
thus better than chance at an S.O.A. of 20 ms. are guessing, and are not conscious of seeing whose
However, at this S.O.A., the subjects were not face has been shown, macaque inferior temporal
conscious of seeing the face, or of the identity of the cortex neurons provide small but significant
face,andfeltthattheirguessingaboutwhichfacehad amounts of information about which face has been
been shown was not correct. The subjects did know shown. When the S.O.A. was increased to 40 ms,
that something had changed on the screen (and this the inferior temporal cortex neurons responded for
was not just brightness, as this was constant approximately 50 ms, and encoded approximately
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0.14 bits of information (in a period of 200 ms, the reason why it may be useful to not interrupt it
for the subset of face-selective neurons tested, unless there is a definite signal that may require the
see Rolls et al., 1999). At this S.O.A., not only use of the type of processing that can be performed
was face identification 97% correct, but the subjects by the conscious processing system, is left to the end
were much more likely to be able to report oftheDiscussionbecausetheissuesraisednecessarily
consciously seeing a face and/or whose face had involve hypotheses that are not easy to test.
been shown. One way in which the conscious Theresultsoftheinformationanalysis(Rollsetal.,
perception of the faces was measured quantitatively 1999) emphasise that very considerable information
was by asking subjects to rate the clarity of the about which stimulus was shown is available in a
faces.Thiswasasubjectiveassessmentandtherefore shortepochof,forexample,50ms.Thisconfirmsthe
reflected conscious processing, and was made using findings of Tove´e et al. (1993), Tove´e and Rolls
magnitude estimation. It is shown in Fig. 7 that the (1995) and Heller et al. (1995), and facilitates the
subjective clarity of the stimuli was low at 20 ms rapid read-out of information from the inferior
S.O.A., was higher at 40 ms S.O.A., and was almost temporal visual cortex, and the use of whatever
complete by 60 ms S.O.A. informationisavailableinthelimitedperiodoffiring
It is suggested that the threshold for conscious under backward masking conditions. It was notable
visual perception may be set to be higher than the that the information in the no mask condition did
level at which small but significant sensory informa- outlast the end of the stimulus by as much as
tion is present so that the systems in the brain that 200–300 ms, indicating some short term memory
implement the type of information processing trace property of the neuronal circuitry. This
involved in conscious thoughts is not interrupted by continuing activity could be useful in the learning
smallsignalsthatcouldbenoiseinsensorypathways. of invariant representations of objects (Rolls, 1992,
Consideration of the nature of this processing, and 2000a;WallisandRolls,1997;RollsandDeco,2002).
TheresultsalsoshowthatevenattheshortestS.O.A.
10 of 20 ms, the information available was on average
0.06 bits. This compares to 0.3 bits with the 16 ms
stimulusshownwithoutthemask(Rollsetal.,1999).
8
Normal It also compares to a typical value for such neurons
Target clarity (mean rating) 46 o(ro2aTe2vffs%aotu0ihv.ll3taea´ose5btft–lahe0atvuh.nfa5sardiotlsbamhwiRbtosliowenthwlelwtsuiha,tirthaoh51tnoa09ca0u9o5lt5n0mr;as0eissdRmmpseootarsialnsmlksbsstue,liesmleautinenusvdflapueolanrs.r,epmpsupe1arnrn9etodist9oxeae7inrntm)it.ob(aa3natTt3i)ceo%hklinyes-
wardmaskingconditionswhichallowtheneuronsto
2
havetheirmainresponsein30ms.Also,wenotethat
the information available from a 16 ms unmasked
0 stimulus (0.3 bits) is a large proportion (approxi-
20 40 60 80 100 120 140 160 180 200 mately 65–75%) of that available from a 500 ms
Stimulus Onset Asynchrony (msec) stimulus.
These results provide evidence on how rapid
Fig.7. Ratingofthesubjectiveclarityoffacesasafunctionof
the processing of visual information is in a cortical
stimulus onset asynchrony (S.O.A.). The mean of the magni-
tudeestimationratingsisshown.(Theclarityoftheface,when area, and provides a fundamental constraint for
presentedwithout being followed by a masking stimulus, was understanding how cortical information processing
assignedthenumber10.Iftheobserverwasnotabletoseethe operates(seeRollsandTreves,1998;RollsandDeco,
featuresoftheface,thatwastobeconsidered0.Theobservers
2002).Onedirectimplicationofthe30msfiringwith
assigned a number from 0 to 10 to represent the perceived
the 20 ms S.O.A. is that this is sufficient time both
subjective clarity of the face. The effect of S.O.A. was
statisticallysignificantatP<0.001.AfterRollsetal.,1994.) for a cortical area to perform its computation, and
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for the information to be read out from a cortical visualsystemaresufficientlyrapidtoallowrecurrent
area, given that psychophysical performance is 50% feedback attractor operations to contribute usefully
correctatthisS.O.A.Anotherimplicationisthatthe toinformationprocessinginthesystem(Panzerietal.,
recognition of visual stimuli can be performed using 2001; Rolls and Deco, 2002; contrast with Thorpe
feedforward processing in the multi-stage hier- et al., 1996).
archicallyorganizedventralvisualsystemcomprising The inferior temporal visual cortex is an appro-
at least V1–V2–V4-Inferior Temporal Visual Cortex, priate stage to analyse the identification of objects
in that the typical shortest neuronal response and faces, and to link to face identification in
latencies in macaque V1 are approximately 40 ms, humans, because the ITC contains an invariant
andincreasebyapproximately15–17msperstageto representationoffacesandobjects(BoothandRolls,
produce a value of approximately 90 ms in the 1998; Rolls, 2000a; Rolls and Deco, 2002), and
inferior temporal visual cortex (Rolls and Deco, damage to corresponding areas in humans may
2002; Oram and Perrett, 1992; Dinse and Kruger, producefaceandobjectagnosias(Farah,1990;Farah
1994; Raiguel et al., 1989; Vogels and Orban, 1994; et al., 1995a,b).
Nowak and Bullier, 1997). (The fact that consider- Thequantitativeanalysesofneuronalactivityinan
able information is available in short epochs, of for areaoftheventralvisualsysteminvolvedinfaceand
example20ms,ofthefiringofneuronsprovidespart object identification described here which show that
of the underlying basis for this rapid sequential significant neuronal processing can occur that is
activation of connected visual cortical areas (Tove´e sufficient to support forced choice but implicit
andRolls,1995;RollsandDeco,2002).)Giventhese (unconscious) discrimination in the absence of
timings,itwouldnotbepossibleinthe20msS.O.A. conscious awareness of the identity of the face is
condition for inferior temporal cortex neuronal of interest in relation to studies of blindsight
responses to feedback to influence V1 neuronal (Weiskrantz et al., 1974; Weiskrantz, 1997, 1998;
responses to the test stimulus before the mask StoerigandCowey,1997;deGelderetal.,1999).The
stimulusproduceditseffectsontheV1neurons.This issue in blindsight is that conscious reports that a
showsthatatleastsomerecognitionofvisualstimuli stimulus has been seen cannot usually be made, and
is possible without top–down backprojection effects yet some forced choice performance is possible with
from the inferior temporal visual cortex to early respect to, for example, the motion, position and
cortical processing areas. some aspects of the form of the visual stimuli. It has
Theprocessingtimeallowedforeachcorticalarea beenarguedthattheresultsinblindsightarenotdue
to perform useful computation and for the informa- just to reduced visual processing, because some
tion to be read out to the next stage of cortical aspects of visual processing are less impaired than
processing is in the order of 15–17 ms as shown by others(Weiskrantz,1997,1998,2001;Azzopardiand
theneuronalresponselatencyincreasesfromcortical Cowey, 1997). However, it is suggested that some of
areatocorticalareanotedabove;andlessthan30ms the visual capacities that do remain in blindsight
as shown by the duration of the firing in the 20 ms reflect processing via visual pathways that are
S.O.A. condition when face identification was 50% alternatives to the V1 processing stream
better than chance. This is sufficient for recurrent (Weiskrantz, 1997, 1998, 2001). If some of those
collaterals to operate by feedback within a cortical pathways are normally involved in implicit process-
area to allow them to implement attractor-based ing, this may help to give an account of why some
processing, as shown by analyses of the speed of implicit (unconscious) performance is possible in
settling of such networks provided that they are blindsight patients. Further, it has been suggested
implementedwithneuronswithcontinuousdynamics that ventral visual stream processing is especially
(as implemented in models by integrate-and-fire involved in consciousness, because it is information
neurons) and with spontaneous firing (Treves, 1993; about objects and faces that needs to enter a system
Battaglia and Treves, 1998; Rolls and Treves, 1998). to plan actions (Milner and Goodale, 1995; Rolls
Indeed, the dynamics of a four-layer hierarchical and Deco, 2002); and the planning of actions that
network with an architecture like that of the ventral involves the operation and correction of flexible
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one-timemultiple-stepplansmaybecloselyrelatedto at which small but significant sensory information is
conscious processing (Rolls, 1999; Rolls and Deco, presentsothatthesystemsinthebrainthatimplement
2002). In contrast, dorsal stream visual processing the type of information processing involved in
maybemorecloselyrelatedtoexecutinganactionon conscious thoughts are not interrupted by small
an object once the action has been selected, and the signals that could be noise in sensory pathways, and
details of this action execution can take place impli- thatmaynotrequireuseofthetypeofprocessingthat
citly (unconsciously) (Milner and Goodale, 1995; canbeperformedbytheconsciousprocessingsystem.
Rolls and Deco, 2002), perhaps because they do not Theexactnatureoftheinformationprocessingthatis
requiremultiplestepsyntacticplanning(Rolls,1999). linked essentially to consciousness is the subject for
The implication of this discussion is that in great debate. My own theory is that phenomenal
blindsight the dissociations between implicit and consciousness is the state that occurs when one is
explicit processing may arise because different visual thinkingaboutone’sownsyntactic(ormoregenerally
pathways, some involved in implicit and others in linguistic)thoughts(Rolls,1999,2000b,1997).Inthat
explicit processing, are differentially damaged. In thetheoryispremisedonthoughtsaboutthoughts,it
contrast, in the experiments described here, the is a Higher Order Thought (HOT) theory of
dissociation between implicit and explicit processing consciousness (see also Rosenthal, 1990, 1993), and
appearstoarisefromallowingdifferentialprocessing in that the theory is about linguistic thoughts, the
(short information-poor versus longer) in the same authorhastermeditaHOLTtheoryofconsciousness
visual processing stream and even area, the inferior (Rolls, 1999, 2000b). It may also be called a HOST
temporal visual cortex. Thus the implications of the theory, as the higher order thoughts are about
dissociations described here, and their underlying syntactic thoughts. The computational argument
neuronal basis, may be particularly relevant in a that the author put to specify why the higher order
different way to understanding visual information thoughts are computationally useful if they are
processing and consciousness. syntactic is as follows. If a multi-step plan involves
One of the implications of blindsight thus seems a number of different symbols, and requires the
to be that some visual pathways are more involved relations (e.g., the conditional relations) between
in implicit processing, and other pathways in thesymbolstobespecifiedcorrectlyineachstepofthe
explicit processing. In contrast, the results described plan, then some form of syntax is needed; for
here suggest that short and information-poor otherwise, the symbols would not be bound together
signals in a sensory system involved in conscious correctlyineachstepoftheplan.Iftheplanproduces
processing do not reach consciousness, and do not an incorrect outcome, then a process that can reflect
interrupt ongoing or engage conscious processing. onandevaluateeachstepoftheplan,anddetermine
Thisevidencedescribedherethusprovidesinteresting whichmaybetheincorrectstep,isawaytosolvethe
and direct evidence that there may be a threshold credit assignment problem (Rolls, 1999). It is argued
foractivityinasensorystreamthatmustbeexceeded thatitisimplausiblethatsuchhigherordersyntactic
in order to lead to consciousness, even when thoughtprocesseswouldoccurwithoutitfeelinglike
that activity is sufficient for some types of visual something to be the system that implements these
processing such as visual identification at well above processes,especiallywhenthethoughtsaregrounded
chance in an implicit mode. The latter implicit mode in the world (Rolls, 1999). This is only a plausibility
processing can be revealed by forced choice tests argument. It should be noted that the higher order
and by direct measurements of neuronal responses. thoughts are linguistic in the sense that they require
(Complementaryevidenceatthepurelypsychophysi- syntax, but not necessarily, of course, human verbal
cal level using backward masking has been obtained language. However, to the extent that some form of
by Marcel (1983a,b) and discussed by Weiskrantz syntactic processing is closely related to conscious-
(1998,2001).)Possiblereasonsforthisrelativelyhigh ness,itislikelytobethataserialandtime-consuming
thresholdforconsciousnessareconsiderednext. processisneeded(withserialprocessingusedtolimit
It is suggested that the threshold for conscious thebindingproblemtowhateversyntaxthebraincan
visualperceptionmaybesettobehigherthanthelevel implement). Given the serial nature of this process,