Download Neuronal mechanisms for the perception of ambiguous stimuli

433
Neuronal mechanisms for the perception of ambiguous stimuli
Andrew J Parker and Kristine Krug
Ambiguous figures that may take on the appearance of two or
more distinct forms have fascinated philosophers and
psychologists for generations. Recently, several laboratories
have studied the neuronal basis of perceptual appearance at the
level of single neurons in the cerebral cortex. Experiments that
integrate neuronal recording with analyses based on sensory
detection theory reveal a remarkable degree of specificity in
these neuronal responses. The new challenges are to
understand how cognitive processes, such as attention and
memory, interact with perception to generate these neuronal
signals.
Addresses
University Laboratory of Physiology, Parks Road, Oxford, OX1 3PT, UK
e-mail: [email protected]
Current Opinion in Neurobiology 2003, 13:433–439
This review comes from a themed issue on
Sensory systems
Edited by Clay Reid and King-Wai Yau
0959-4388/$ – see front matter
ß 2003 Elsevier Ltd. All rights reserved.
DOI 10.1016/S0959-4388(03)00099-0
Abbreviations
fMRI functional magnetic resonance imaging
Introduction
‘I contemplate a face, and then suddenly notice its likeness
to another. I see that it has not changed; and yet I see it
differently. (The) causes are of interest to psychologists.’
Ludwig Wittgenstein Philosophical Investigations [1].
Many figures change in a discrete and salient way during
viewing. The quotation highlights the experience of
suddenly appreciating the resemblance of one figure to
another. When this happens, the figure that we are viewing does not change materially, yet the significance of
features in the figure is altered by our cognitive processes.
The most intriguing figures of this type are perceptually
ambiguous. Such figures provide the experience of looking
at a constant external stimulus whose perceptual appearance changes from one viewing to the next, or indeed from
one moment to the next in continuous viewing. Figures of
this type have fascinated philosophers and psychologists
for generations because they offer insight into the cognitive, mental processes of perception. Neuroscientists
have the same motivation as earlier scholars. Examples
www.current-opinion.com
of current interest are found in binocular rivalry [2,3],
perception of three-dimensional shapes [4–7], motion
perception [8] and figure–ground relationships [9,10].
The study of how the brain responds to a shift in the
perceptual appearance of a figure provides insights into
neuronal processes that are crucially associated with
perceptual decision-making. In the ideal case, the neuronal signals do indeed reflect the shift in perceptual
appearance, because the external stimulus delivered to
the sensory receptors remains the same. Thus, (it is
argued) these particular neuronal signals reflect a form
of mental processing that is ‘higher’ or ‘deeper’ than
simple detection and analysis of the external sensory
stimulus. Such processing may reflect the influence of
experience in the form of memory and cognition. More
speculatively, the neuronal signals could reflect conscious
perception or even an ‘act of will’ in taking up one
perceptual interpretation rather than another. Such interpretations would elevate the neuronal signals under study
to ‘neuronal correlates of consciousness’ [11–14].
Exciting although such interpretations may be, there are
numerous obstacles in the way of moving forward with
this programme of work. Nonetheless, we argue here that
the past few years have seen some striking advances in
the identification of neuronal signals related to perception. Improved knowledge about the sources and sites of
these signals has come from the steady application of
single-unit recording and, more recently, the use of new
technologies (functional magnetic resonance imaging
[fMRI], magneto-encephalography and other brain imaging). The development of novel behavioural paradigms
(particularly for application with non-human subjects) has
enabled a new range of studies at the level of single
neurons. In conjunction with these advances, it has been
proposed that one might be able to use perceptual paradigms, such as multistable figures, as a psychobiological
probe of cognitive traits associated with affective or other
mood disorders in humans [15].
The simple identification of a physiological signal as a
putative ‘neuronal correlate of perception’ is less novel
and newsworthy as a research result than it once was.
Significantly, our understanding of perceptually relevant
signals has developed considerably with new theoretical
approaches. Psychophysical and neurophysiological studies that employ rigorous statistical methods for analysing
performance in making sensory decisions [16] provide
powerful results that are now being used in the study of
perceptual ambiguity. This is exerting a drive towards
finding answers that provide a quantitative account of
Current Opinion in Neurobiology 2003, 13:433–439
434 Sensory systems
firing patterns within populations of cortical neurons.
Second, investigators are now beginning to think about
the relationships among the particular signals that correlate with perceptual decisions when subjects view ambiguous figures and the more general neuronal signals that
are involved in perceptual and cognitive decisions. For
example, neuronal mechanisms that underlie attention
have been studied in depth in the past few years [17–19],
and an important future activity is to determine how the
signals identified in the attention paradigm relate to those
identified in perceptual decision-making [20].
As the focus here is on sensory decision-making, positive
emphasis in selecting papers for discussion has been
given to experiments that measure signals at the level
of single neurons and small neuronal populations rather
than at the level of cortical areas or regions. Consequently, we feature most strongly the responses of neurons in non-human primates that have been trained to
make perceptual judgments about perceptually ambiguous stimuli. The extensive literature that uses the
technique of human brain imaging is discussed mainly
as a source for correlative information.
Multistable figures
There are many examples of multistable figures. Normally, these figures may be seen in one of two different
configurations, although some have more than two possibilities. At any one time, the configuration that is
dominant excludes or suppresses the perception of the
alternative configurations. The quotation at the beginning reminds us that this experience of perceiving distinct
configurations is not unique to multistable figures. What
is particularly characteristic about multistable figures is
that the different configurations possess roughly equal
saliency or power to dominate perception.
True rivalry, as in binocular rivalry, involves something
that is physically present but not perceived (the supFigure 1
Current Opinion in Neurobiology
The Necker cube is a classic example of a perceptually reversible
figure [47].
Current Opinion in Neurobiology 2003, 13:433–439
Figure 2
(View from above)
Negative
disparity
Zero
disparity
Positive
disparity
Ambiguous
rotation
CW or CCW
CW
rotation
(Appearance)
CCW
rotation
Current Opinion in Neurobiology
A schematic to show how the combination of dot movement and dot
disparity defines the direction of rotation of the cylinder. The movement
of the dots on a computer screen defines a rotating cylinder. The
direction of rotation can only be resolved if the rightward moving dots
can be determined to lie on the either the front or rear surface. Thus,
rightward motion on the rear surface implies clockwise (CW) rotation (as
viewed from above) and the opposite implies counter-clockwise (CCW)
rotation. This can be achieved by giving the rightward moving dots a
binocular disparity with respect to the leftward moving dots (see CW and
CCW rotation at left and right of figure). Perceptually ambiguous
cylinders (centre of figure) are composed of dots all with the same
binocular depth. Their movement is equally consistent with CW and
CCW rotations. Even a slight excess of dots moving in one direction
cannot remove this ambiguity in the stimulus. (Adapted from [40]).
pressed stimulus). In contrast, in a figure such as the
Necker cube (Figure 1) or the cylinder paradigm that we
discuss in detail later (Figure 2), the entire stimulus
configuration is consumed by one perceptual interpretation, leaving nothing residual the perception of which is
suppressed. Neuronal responses to suppressed stimuli
have been studied with a specific paradigm of flash
suppression as well as with binocular rivalry. In both
paradigms, suppressed stimuli provide one index of
whether or not neuronal firing is directly linked with
conscious perception of objects. If neurons continue to
fire to suppressed stimuli, then it is argued that they
cannot be directly involved in conscious perception
[21,22]. Indeed, some neurons are reported as becoming
more active when their preferred stimulus (as assessed
with unambiguous stimuli) is suppressed [2,23].
With figures such as the Necker cube, the two interpretations form distinct complementary categories and the
instability lies at the boundary of these categories. As
in the binocular rivalry paradigm, it is natural to interpret
www.current-opinion.com
Neuronal mechanisms for the perception of ambiguous stimuli Parker and Krug 435
the instability as the alternating dominance of one of a
pair of neuronal populations. Specifying the nature of the
neuronal signals that reflect this dominance is a goal of
current research. We would like to know the location, size
and composition of the two hypothesized neuronal populations, the identity of the signals that are present during
dominant and non-dominant phases, the way that those
signals are distributed within the population and whether
or not there is a unique neuronal signature associated with
the moment of switching from one perceptual interpretation to another.
These questions are currently approached with two main
types of paradigm. In continuous viewing, the ideal
situation is to obtain a lengthy period during which the
subject views a multistable figure and reports which
percept dominates at any one time. Simultaneous neuronal recordings are made so that the temporal correlation
of neuronal and perceptual changes can be assessed. In
the other paradigm, a multistable figure is presented for a
single fixed duration (much shorter than the average
switching time in continuous viewing) and the subject
is required to choose one of two alternatives to make a
perceptual report at the end of the trial. Again, a correlation of neuronal activity and perceptual decision is the
measured outcome.
Precision of neuronal correlates of
perception
Although this account is straightforward, real applications of these paradigms are considerably more complex.
Most of the reasons for this complexity arise from the
fact that these measures are simply correlations. Unless
several rigorous controls are conducted, there is always
the danger that the underlying cause of the correlations
measured in a particular neuronal population may actually arise from the activity of a third neuronal population
in which activity has not been monitored. This third
population might not even be connected anatomically
with the neurons from which recordings have been
made. For example, if a subject makes a characteristic
eye movement in association with a particular perceptual
decision, then that eye movement may generate changes
in the retinal image that affect populations of visual
neurons that are unrelated to the perceptual decisions.
Although changes of this type are often classed as
spurious, it should be recognized that they must inevitably form a component of the brain’s responses during
natural viewing, such as looking informally at multistable figures.
A complementary issue regarding correlation measures is
that they can easily be diluted by measurement error. For
example, if the subject does not report the percepts
honestly, these inaccuracies will dilute correlations that
ought to have been revealed. This problem is most acute
when working with non-human primates whose behavwww.current-opinion.com
ioural strategy is to exploit the experimental paradigm to
maximise the delivery of rewards. However, human
observers are not immune from these lapses, particularly
during the long periods of observation that are needed
either to characterize some types of perceptual switch or
to collect the slow haemodynamic responses in fMRI
experiments. The main approach to combat these lapses
is to include ‘catch trials’, in which unambiguous stimuli
are presented so that the honesty of the observer can be
evaluated. For this approach to be completely effective,
there should be no perceptual difference between an
ambiguous stimulus that is currently engendering one
perceptual state and the unambiguous stimulus that
corresponds to that perceptual state.
A related issue is raised by the use of behavioural measures that substitute for perceptual reports. For example,
the way in which the eyes follow the movement of
individual components of a pair of binocularly rivalrous
patterns is strongly linked to whichever pattern is perceptually dominant at any one time. This means that
optokinetic responses can be used as an ersatz index of
perceptual dominance without the need to train animals
to respond behaviourally [24–26]. Although the correlation between perceptual reports and eye movements is
high, it is not perfect [24], for reasons that are not wholly
clear. It should not be automatically assumed that the
perceptual reports are perfect and that the problem lies
with the substitute measure that is formed on the basis of
eye movements. Whatever the case, this is another factor
that can dilute correlations between neuronal signals and
perceptual dominance.
Sites of perceptual decision-making
At the neuronal level, the continuous viewing paradigm
has largely been used in connection with binocular rivalry
or the related paradigm of flash suppression [2,3,11,22,
27]. The emerging view is that the neuronal correlates of
binocular rivalry are widely dispersed throughout many
areas of the visual cortex and beyond. A similar observation has been made for rivalrous motion stimuli [28].
On the one hand, this observation is arguably unsurprising from the viewpoint that the relevant neuronal site
that causes the change in percept is early in the visual
pathways: all sites deeper in the pathway will reflect
the modulation by these earlier neurons. On the other
hand, it is also possible to sustain an argument that the
causally relevant site(s) for rivalry may be deep in the
pathways: according to this view, the modulation seen in
earlier areas is a correlate of the activation derived from
sites deep in the cortex that send feedback to earlier sites.
Finally, there is a third perspective on rivalry that
attempts to take a middle way: here it is argued that
the competitive nature of interactions among neuronal
populations is played out simultaneously at multiple
levels within the nervous system. In all three cases,
Current Opinion in Neurobiology 2003, 13:433–439
436 Sensory systems
the argument can be made that sites showing signs of
perceptual modulation ought to be dispersed throughout
wide regions of the visual brain.
Some ways of breaking this deadlock are therefore
required. In the case of binocular rivalry, interest has
centred on the question of whether or not the rivalry is
truly eye-related (early) or percept-related (late) [3,27,
29,30,31]. It is increasingly clear that both forms of rivalry
may be predominant under different conditions. In one
recent example, Bonneh et al. [32] used composite
stimuli with Gabor patches of aligned or random orientations. (A Gabor patch is a small oriented feature whose
spatial luminance profile is formed by the multiplication
of a sinusoidal waveform with a Gaussian envelope.)
Orientation jitter breaks up any pattern, therefore favouring eye-rivalry rather than percept-rivalry. There is a
gradual shift from eye-rivalry to percept-rivalry as pattern
coherence is increased, thus a reconciliation of apparently
conflicting results is offered.
Several avenues now need to be pursued. First, the
timing relationships among the perceptually related signals that are found in different cortical areas need to be
explored. Relevant neuronal activity often occurs in
advance of the perceptual report by up to 1 s [2], but
the greatest precedence should clearly be accorded to
sites with the earliest activity. This will require recordings to be made simultaneously from multiple neurons
within identified brain areas and from multiple brain
areas. Some recent studies highlight the potential complexity of events when switches occur in binocular rivalry. Wilson et al. [33] placed a conventional binocular
rivalry stimulus in the spatial form of a thin-ringed
annulus. They observed that the switch of visibility from
one stimulus to the other propagated systematically
around the annulus. They were able to estimate the
speed of propagation, and proposed that this might
reflect the dynamics of a physiological process that travels across the cortical surface. The neuronal correlates of
such a process would inevitably have a complex time
structure. A parallel issue has also been reported in the
featural domain [34], in which a disjunction between the
rivalry of orientation and motion direction has been
observed (see also [35]). Thus, neurons selective for
orientation but not selective for motion direction might
have a time-course of activations that reflect the perceptual rivalry attached to orientation, whereas neurons
selective for direction of motion might have a different
time-course that reflects the temporal sequence of perceptual changes in motion direction.
Second, sites in which sensory evidence and decisionrelated activity converge also need detailed examination.
In normal situations, perceptual decisions are based on a
combination of prior knowledge and evidence about the
current state of the world. Brain sites that actually play a
Current Opinion in Neurobiology 2003, 13:433–439
central role in perceptual decisions should show signs of
integrating these two types of signal. Specifically, in
considering ambiguous stimuli, the most interesting brain
sites are those that represent both alternatives but have a
preponderance of activity in favour of the perceptual
decision when the ambiguous stimulus is presented. Sites
that represent only the perceptual decision to the complete exclusion of the alternative would presumably be
post-decision, whereas sites that reflect only the external
stimulus with no decision-related activity are also of little
explanatory value.
Third, and most crucially, there need to be attempts to
intervene causally in the decision-making process. Unfortunately, the range of techniques that are of value here is
limited. Ideally an intervention should act in some specific way, such as shifting the pattern of perceptual reports
in favour of one alternative without otherwise disrupting
perceptual performance or specifically changing the rate
of alternation [15]. The most promising approach is
electrical microstimulation, which has been used successfully to intervene in the formation of sensory decisions by
the application of focal activation to small groups of
neurons and their connections [36,37]. Another possibility
would be the brief and reversible application of pharmacological agents.
Forcing a decision
A different approach to monitoring responses to perceptually ambiguous stimuli is to make stimulus presentations of fixed duration that require a decision at the end of
the presentation. The duration must be short, so that
there is a very small chance of instability during the single
presentation. Although there is then no chance of examining the neuronal responses to perceptual switches, there
are several compensating advantages, which are illustrated by the use of ambiguous structure-from-motion
stimuli [4,5,38,39,40,41].
These stimuli depict rotating spheres or cylinders by
means of a pattern of random dots in motion (see
Figure 2). The dots are arranged on two transparent
superimposed surfaces and the movement of the dots
is consistent with a global rotation of the figure. The
ambiguity of these figures lies in the fact that any
particular pattern of dot movements is by itself consistent with either one or the other of the two possible
directions of rotation. A set of dots that is moving rightwards on a vertically oriented cylinder rotating about its
principal axis is consistent with a clockwise rotation of
the cylinder if the dots are on the rear surface but a
counter-clockwise rotation if the dots are on the front
surface. The ambiguity can be resolved by adding binocular stereoscopic disparity to the display. Front and rear
can then be defined by separating the rightward and
leftward moving dots in binocular depth so that the
direction of rotation is fixed.
www.current-opinion.com
Neuronal mechanisms for the perception of ambiguous stimuli Parker and Krug 437
The main advantage is that it becomes much easier to
embed ambiguous stimuli as relatively rare events within
a sequence of trials that are mostly unambiguous. As the
behavioural response on unambiguous trials is always
right or wrong, this provides a way of probing the honesty
of the subject’s responses. Indeed, if the set of unambiguous stimuli is placed in the range of the sensory detection threshold for stereo disparity [40], it becomes
impossible to distinguish unambiguous from ambiguous
stimuli. The only way for the subject to maximise the
proportion of correct responses is to treat all stimuli as
unambiguous and respond accordingly. An important
observation is that the switching times during continuous
viewing are much longer than the one or two second trials
used for fixed-duration presentations (E Brunskill, et al.
unpublished data).
Under these conditions, neurons in the extrastriate cortical area V5/MT exhibit a remarkable degree of specificity in signalling the reported percept with ambiguous
stimuli. V5/MT neurons that show a sensory preference
for clockwise rotation of unambiguous stimuli also show
enhanced firing in response to ambiguous stimuli when
they are reported as having clockwise rotation. This
enhancement of firing represents a tight correlation
between neuron and behaviour, as is shown by the high
values of choice probability in this task [40]. Listening to
the output of just the average neuron in this brain area
during a single trial gives a chance better than 2:1 of
correctly predicting the perceptual choice at the end of
the trial, with some individual neurons showing much
higher reliability.
An important aspect of these recent data is the absence of
neurons that show a sensory preference for one direction
of rotation and a decision-related response to the opposite
direction of rotation. This result differs from earlier
measurements of single-neuron correlates of perception
[2,5,23,41]. There may be two reasons for this. First, in
the binocular rivalry paradigm the perceptually suppressed stimulus is still physically present on the retina
and some neurons respond to it. For the cylinder paradigm, every physically present dot is always accounted
for by the current perceptual interpretation, with no dots
left over. Second, the monkeys in the study by Dodd et al.
[40] were specifically required to work at a psychophysical threshold, which may effect a tighter link between
decision-related firing and behavioural choice, perhaps
through a tighter control of attention.
Decision-making about the perceptual appearance of
the ambiguous stimulus is tightly coupled to the activity
in two sensory pools of neurons. One pool favours clockwise rotation and the other counter-clockwise rotation.
There are two competing hypotheses for enhanced firing
in the currently favoured pool. According to one hypothesis, the fluctuations of firing in sensory signals within
www.current-opinion.com
V5/MT are sufficient to flip perception one way or
another. This event could then be reinforced by a feedback signal that is generated internally within V5/MT and
stabilizes the current perceptual interpretation. With the
other hypothesis, the enhanced firing observed in V5/MT
reflects a perceptually related signal that is derived from
higher-order cortical areas. Both ideas are consistent with
the greater size of choice probabilities for ambiguous
cylinders [40] when compared with random motion [42].
Current thinking places this decision-making process
close to the one that is hypothesized to underlie the sensory discrimination of motion direction [16,42,43] and
binocular disparity [44] in the same cortical area. However, there are some marked differences. Importantly so
far, no positive effect of electrical microstimulation [36,44]
on the perception of ambiguous structure-from-motion
stimuli has been identified. In addition, in the motion and
disparity studies, the neutral stimulus is a field of dots
with a noisy structure, which is qualitatively different
from fields of dots that are all moving in the same
direction (in the motion study) or all at the same depth
plane (in the disparity study). This contrasts sharply with
the two distinct perceptual interpretations for the ambiguous rotating cylinder. The neutral motion stimulus itself
contains random fluctuations that could potentially favour
a particular motion direction, although these fluctuations
are not responsible for driving the correlation of behavioural decision and neuronal activity in the detection of
motion [42]. For the ambiguous cylinder, a momentary
excess of rightward moving dots does not inherently
favour the perception of either clockwise or counterclockwise rotation.
Conclusions
Our best indications are that the resolution of perceptual
ambiguity proceeds at the neuronal level in much the
same way that other perceptual decisions are formed
[45]. The activity of pools of sensory neurons contributes evidence over a time period of decision formation.
This period may be terminated either spontaneously or
by the removal of the stimulus. Alternatively, during
prolonged viewing, the time-period slides continuously
such that the most recent evidence receives the strongest
weighting. The neuronal characteristics that favour perceptual ambiguity within a stimulus are that the activity
levels of two competing pools of sensory neurons are
closely balanced and that the pools represent two, highly
distinct perceptual categories. Even small changes in the
sensory evidence – changes near the psychophysical
threshold – can favour one perceptual state over the
other. Within V5/MT, the correlation of neuronal responses with perceptual choice is numerically larger in
the case of ambiguous stimuli [40] than it is during
discrimination of motion direction [42]. By itself, this might
suggest that decision-related activity with ambiguous stimuli is more tightly focussed within a smaller group of
Current Opinion in Neurobiology 2003, 13:433–439
438 Sensory systems
neurons. Such an interpretation cannot be rejected for
now. However, a serious alternative hypothesis is that
decision-related activity may reflect the neuronal correlates of other cognitive processes, such as attention, as
well as the formation of the decision itself [20,46]. Future
experiments will need to make overt manipulations of
attentional processes to evaluate this issue.
17. McAdams CJ, Maunsell JHR: Effects of attention on the
reliability of individual neurons in monkey visual cortex.
Neuron 1999, 23:765-773.
Acknowledgements
20. Krug K: A common neuronal code for perceptual processes?
Comparing choice and attention signals in cortical area V5/MT.
Phil Trans R Soc Lond B Biol Sci 2003, in press.
Work in our group is supported by the Wellcome Trust, James S McDonnell
Foundation and the Royal Society. K Krug is a Dorothy Hodgkin Fellow of
the Royal Society.
References and recommended reading
Papers of particular interest, published within the annual period of
review, have been highlighted as:
of special interest
of outstanding interest
18. Treue S, Trujillo JCM: Feature-based attention influences
motion processing gain in macaque visual cortex. Nature 1999,
399:575-579.
19. McAdams CJ, Maunsell JHR: Attention to both space and feature
modulates neuronal responses in macaque area V4.
J Neurophysiol 2000, 83:1751-1755.
21. Sheinberg DL, Logothetis NK: The role of temporal cortical areas
in perceptual organization. Proc Natl Acad Sci USA 1997,
94:3408-3413.
22. Kreiman G, Fried I, Koch C: Single-neuron correlates of
subjective vision in the human medial temporal lobe. Proc Natl
Acad Sci USA 2002, 99:8378-8383.
The authors present a study that exploits the rare possibility of recording
directly from single cortical neurons in conscious human subjects.
1.
Wittgenstein L: Philosophical Investigations, edn 3. Translated by
Anscombe GEM. Oxford, UK: Basil Blackwell; 1972.
23. Logothetis NK, Schall JD: Neuronal correlates of subjective
visual-perception. Science 1989, 245:761-763.
2.
Leopold DA, Logothetis NK: Activity changes in early visual
cortex reflect monkeys’ percepts during binocular rivalry.
Nature 1996, 379:549-553.
24. Logothetis NK, Schall JD: Binocular motion rivalry in macaque
monkeys — eye dominance and tracking eye-movements.
Vision Res 1990, 30:1409-1419.
3. Blake R, Logothetis NK: Visual competition. Nat Rev Neurosci
2002, 3:13-23.
An invaluable summary that is written chiefly from the perspective of
rivalrous percepts.
25. Fries P, Schroder JH, Singer W, Engel AK: Conditions of
perceptual selection and suppression during interocular rivalry
in strabismic and normal cats. Vision Res 2001, 41:771-783.
4.
Treue S, Husain M, Andersen RA: Human perception of structure
from motion. Vision Res 1991, 31:59-75.
5.
Bradley DC, Chang GC, Andersen RA: Encoding of threedimensional structure-from-motion by primate area MT
neurons. Nature 1998, 392:714-717.
6.
Orban GA, Sunaert S, Todd JT, Van Hecke P, Marchal G: Human
cortical regions involved in extracting depth from motion.
Neuron 1999, 24:929-940.
7.
Paradis AL, Cornilleau-Peres V, Droulez J, Van de Moortele PF,
Lobel E, Berthoz A, Le Bihan D, Poline JB: Visual perception of
motion and 3-D structure from motion: an fMRI study.
Cereb Cortex 2000, 10:772-783.
8.
Muckli L, Kriegeskorte N, Lanfermann H, Zanella FE, Singer W,
Goebel R: Apparent motion: event-related functional magnetic
resonance imaging of perceptual switches and states.
J Neurosci 2002, 22:RC219.
9.
Hasson U, Hendler T, Ben Bashat D, Malach R: Vase or face? A
neural correlate of shape-selective grouping processes in the
human brain. J Cogn Neurosci 2001, 13:744-753.
10. Andrews TJ, Schluppeck D, Homfray D, Matthews P, Blakemore C:
Activity in the fusiform gyrus predicts conscious perception of
Rubin’s vase-face illusion. Neuroimage 2002, 17:890-901.
11. Logothetis NK: Single units and conscious vision. Philos Trans R
Soc Lond B Biol Sci 1998, 353:1801-1818.
12. Ffytche D: Neural codes for conscious vision. Trends Cogn Sci
2002, 6:493-495.
13. Moutoussis K, Zeki S: The relationship between cortical
activation and perception investigated with invisible stimuli.
Proc Natl Acad Sci USA 2002, 99:9527-9532.
26. Fries P, Schroder JH, Roelfsema PR, Singer W, Engel AK:
Oscillatory neuronal synchronization in primary visual cortex
as a correlate of stimulus selection. J Neurosci 2002,
22:3739-3754.
27. Polonsky A, Blake R, Braun T, Heeger DJ: Neuronal activity in
human primary visual cortex correlates with perception during
binocular rivalry. Nat Neurosci 2000, 3:1153-1159.
28. Sterzer P, Russ MO, Preibisch C, Einschmidt A: Neural correlates
of spontaneous direction reversals in ambiguous apparent
visual motion. Neuroimage 2002, 15:908-916.
29. Logothetis NK, Leopold DA, Sheinberg DL: What is rivalling during
binocular rivalry? Nature 1996, 380:621-624.
30. Lee SH, Blake R: Rival ideas about binocular rivalry. Vision Res
1999, 39:1447-1454.
31. Tong F, Engel SA: Interocular rivalry revealed in the human
cortical blind-spot representation. Nature 2001, 411:195-199.
An ingenious study that exploits the monocular representation of the
blind-spot in the primary visual cortex to study the fMRI signals associated with a switch in visibility in binocular rivalry.
32. Bonneh Y, Sagi D, Karni A: A transition between eye and object
rivalry determined by stimulus coherence. Vis Res 2001,
41:981-989.
This study makes a test of the hypothesis about pattern rivalry by
specifically manipulating the coherence of oriented regions in the rivalrous patterns.
33. Wilson HR, Blake R, Lee SH: Dynamics of travelling waves in
visual perception. Nature 2001, 412:907-910.
34. Andrews TJ, Blakemore C: Integration of motion information
during binocular rivalry. Vision Res 2002, 42:301-309.
14. Rees G, Kreiman G, Koch C: Neural correlates of consciousness
in humans. Nat Rev Neurosci 2002, 3:261-270.
35. van de Grind WA, van Hof P, van der Smagt MJ, Verstraten FAJ:
Slow and fast visual motion channels have independent
binocular-rivalry stages. Proc R Soc Lond B Biol Sci 2001,
268:437-443.
15. Pettigrew JD, Miller SM: A ‘sticky’ interhemispheric switch in
bipolar disorder? Proc R Soc Lond B Biol Sci 1998,
265:2141-2148.
36. Salzman CD, Britten KH, Newsome WT: Cortical
microstimulation influences perceptual judgments of motion
direction. Nature 1990, 346:174-177.
16. Parker AJ, Newsome WT: Sense and the single neuron: probing
the physiology of perception. Annu Rev Neurosci 1998,
21:227-277.
37. Gold JI, Shadlen MN: The influence of behavioral context on the
representation of a perceptual decision in developing
oculomotor commands. J Neurosci 2003, 23:632-651.
Current Opinion in Neurobiology 2003, 13:433–439
www.current-opinion.com
Neuronal mechanisms for the perception of ambiguous stimuli Parker and Krug 439
38. Ullman S: The Interpretation of Visual Motion. Cambridge,
Massachusetts: MIT Press; 1979.
39. Bradley DC, Qian N, Andersen RA: Integration of motion and
stereopsis in middle temporal cortical area of macaques.
Nature 1995, 373:609-611.
43. Britten KH, Shadlen MN, Newsome WT, Movshon JA: The
analysis of visual-motion — a comparison of neuronal
and psychophysical performance. J Neurosci 1992,
12:4745-4765.
44. DeAngelis GC, Cumming BG, Newsome WT: Cortical area MT
and the perception of stereoscopic depth. Nature 1998,
394:677-680.
40. Dodd JV, Krug K, Cumming BG, Parker AJ: Perceptually bistable
figures lead to high choice probabilities in cortical area MT.
J Neurosci 2001, 21:4809-4821.
The authors find that during perceptual judgements about ambiguous
figures, V5/MT contains decision signals that are statistically strong and,
importantly, specific to the way that the neuron responds to unambiguous
figures.
45. Gold JI, Shadlen MN: Banburismus and the brain: decoding the
relationship between sensory stimuli, decisions, and reward.
Neuron 2002, 36:299-308.
The authors present a synthesis of recent advances in understanding how
neuronal pools contribute to the formation of perceptual decisions.
41. Grunewald A, Bradley DC, Andersen RA: Neural correlates of
structure-from-motion perception in macaque V1 and MT.
J Neurosci 2002, 22:6195-6207.
46. Parker AJ, Krug K, Cumming BG: Neuronal activity and its links
with the perception of multi- stable figures. Philos Trans R Soc
Lond B Biol Sci 2002, 357:1053-1062.
42. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA:
A relationship between behavioral choice and the visual
responses of neurons in macaque MT. Vis Neurosci 1996,
13:87-100.
47. Wheatstone C: Contributions to the physiology of vision: II. On
some remarkable, and hitherto unobserved, phenomena of
binocular vision (continued). Philos Trans R Soc Lond 1852,
142:1-17.
www.current-opinion.com
Current Opinion in Neurobiology 2003, 13:433–439