Three recent publications (Del Cul et al., 2007; Melloni et al., 2007,
and Quiroga et al., 2008) present a wealthy of psychophysical data,
creating an ‘embarass de richesse" in the study of neural correlates
of visual consciousness.
A first controversy, derived from a comparison of the results, is if
conscious processing is supported by sparse activity (increase of
spike rates in relatively few neurons) or by the excitation of large
neural assemblies. A second controversy is if consciousness is based
on dendritic activity (synchronous oscillations of post-synaptic
potentials, as – roughly – recorded by the EEG) or axonal activity
(neuron firing, as recorded by single and multi-unit recordings). A
third controversy is if visual consciousness is generated by a earlier
synchronous phase (around 80-130 ms after stimulus onset) or later
ones (above 270 ms after stimulus onset).
The possible existence of too many correlates of visual consciousness
requires theoretical integrative work to solve apparent conflict and
create a new synthesis of results. In this review, after briefly
noticing the most relevant results, I summarize a chronology of brain
events correlated to conscious visual processing.
The study of visual consciousness in cognitive neuroscience is based
on establishing correlations between three parameters: properties of
visual stimuli, brain activity and the conscious state of the subject.
Del Cul et al. (2007) used a new methodology to sharpen the control of
visual stimuli: the presentation of supraliminar stimuli combined with
backward masking. The main goal was to find the sequence of brain
events necessary for the formation of a reportable conscious visual
state. The target stimulus consisted of a single digit (a number)
projected for 16 ms (a brief, but supraliminar stimulus). The mask was
a group of numbers projected soon after, for 250 ms, at the same
visual location. The authors varied the time interval (called SOA,
“target-mask stimulus onset asynchrony”) between stimulus onset and
the presentation of the mask, from 16 to 100 ms. Shorter intervals
were predicted to cause backward masking of the stimulus (basically,
relegating the stimulus below the threshold of consciousness), by
means of a perturbation of the sequence of brain events necessary to
generate the corresponding conscious state. Longer intervals would not
perturb the brain processing of the stimulus, allowing the propagation
of excitation to higher cortical areas.
High-density event-related potential (ERP) recordings were collected
to determine whether a change (or a “transition”) in brain activity
occurred between the lower and higher SOA values. The temporal
location of this transition was defined behaviorally, using two
measures: a forced-choice comparison of the presented digit with
another one (checking for both sub- and supraliminar perception), and
a scale of visibility, which assesses the conscious access to the
stimulus. This methodology produced several behavioral and
physiological (ERP) results. Behaviorally, a “significant
nonlinearity” was found for the SOA interval from 33 to 66 ms. Below
16 ms, the performance was at chance level, suggesting that the
presented digit was completely masked by the second. In the 16-33 ms
interval, performance in the forced-choice task was above chance,
while in the 33-66 ms interval both the forced-choice and the
(conscious) visibility ratings increased non-linearly. Above 66 ms
there was not a significant change in visibility and the subjects
consistently had conscious access to the presented stimulus.
The authors looked for ERP components temporally correlated with the
transition in visibility elicited by the 50 ms SOA. Using statistical
testing across subjects, they found activity within a fronto-parieto-
temporal network to be strongly correlated with the non-linear
increase in visibility. The activity that correlates with the
transition occurs about 270 to 300 ms after target onset. This finding
is consistent with the hypothesis that conscious access to a visual
stimulus involves the sequential activation of several cortical
areas.
The second study (Quiroga et al., 2008) has similarities and
differences in methodology with Del Cul. et al. One of the differences
is that Quiroga et al. made single and multi-unit recordings
(measurement of axonal activity by means of invasive microelectrodes
implanted in epilepsy patients), while Del Cul et al. used ERP. The
second difference is that Del Cul et al. measured neural activity
(including both dendritic and axonal signals) in the whole cortex,
while Quiroga was restricted to axonal firing in the medial temporal
lobe. The third difference is that Del Cul et al. presented simple
stimuli for a minimal supraliminar perceptual time duration (one digit
number for 16 ms) while Quiroga presented complex stimuli for longer
and varied times (pictures of faces and buildings during 33 to 264
ms).
The fourth (and central) difference is that the stimulus and mask
durations varied in the Quiroga experiment (while keeping the total
time of stimulus and mask presentation at 500 ms), while Del Cul
varied the time interval between them. In the Del Cul et al.
experiment the frontal response was abolished by shorter time
intervals between stimulus and mask (in this case, there was only
subliminar perception). The Quiroga et al. methodology does not allow
the usage of the masking procedure to check the necessity of medial
temporal responses for visual consciousness (they assume that the
masking procedure only affected occipital visual areas, allowing them
to rule out a crucial role of these areas for visual consciousness).
The results seem to be compatible, because the medial temporal
response measured by Quiroga (at approximately 300 ms after stimulus
onset) occurs simultaneously with or soon after the frontal response
measured by Del Cul et al. (at 270-300 ms). There are, of course,
several possible interpretations of this compatibility:
a) both responses (frontal and medial temporal) occur at the same time
and both support visual consciousness equally. In this case, the key
question is: how does the firing of one or few neurons relate to the
activity of a large synchronized assembly?
b) one of the responses occur first and supports visual consciousness;
the other serves to another function (e.g., the Del Cul et al.
response may be related to short-term memory and the Quiroga et al.
response may be related to triggering the formation of long-term
memory).
Adding to this wealthy of data, another experiment – conducted by
Melloni et al. (2007) – showed an early transient phase, described as
“long-distance synchronization of gamma oscillations across widely
separated regions of the brain”. This synchronized phase occurred from
80 to 120 ms after stimulus presentation. The problem that emerges
from a comparison with Del Cul et al. is if consciousness of the
stimulus really occurred simultaneously to the early synchronization,
since Del Cul et al. discovered that a similar stimulus takes at least
270 ms to be consciously perceived.
Melloni et al. (2007) recorded the EEG during a delayed matching to
sample task in two conditions: the target stimulus, a word – presented
for 33 ms – was preceded and followed by a mask – during 67 ms for
each presentation. The experimenters provided variations in luminance,
that rendered the stimulus visible or invisible (but still processed).
The matching with another word was performed 533 ms after the
presentation of the target. Visible words were correctly recognized in
94,5% of the cases, while the recognition of invisible words was at
chance level (52,2%). However, the behavioral measurement did not
check for conscious perception at the time of the early synchronized
phase; this correlation was induced from the fact that such a phase
only occurred for visible words (for a more accurate description of
the position of the authors, the discussion section of the paper
should be consulted).
A different interpretation of the result could be that the early
synchronous phase is necessary to prepare the conscious visual state,
but this state is completed only later. In this case the early
synchronization would have the function of priming the visual system
for further events. Physiologically, this priming corresponds to a
post-synaptic potentiation process that has to be sustained for a
longer time to participate in the conscious process (see the idea of
“meta-potentiation” proposed by Pereira and Furlan, 2007).
A theoretical integration of results from the three above
papers is actually very complex, for a series of reasons. Synchrony
refers primarily to the oscillation of post-synaptic potentials, but -
as a consequence of local oscillatory synchrony – synchronized firing
can also occur. Such a synchronous firing may be necessary to
broadcast local patterns to other parts of the brain, since the
integration of information required by the conscious process possibly
requires the interplay of local and global activities (Buzsáki, 2007).
Some modalities of oscillatory synchrony possibly requires the
participation of astrocytes (Fellin et al., 2004; Halassa et al.,
2007), developing into a late phase-locking of gamma, alpha e theta
frequencies (as proposed by Palva and Palva, 2007).
A chronology of events that include all relevant and compatible
findings would be the following:
a) Under 80 ms after stimulus onset, stimulus-evoked receptor field
responses occur in primary sensory areas, without conscious perception
of the stimulus;
b) Around 100-120 ms after stimulus onset pre-conscious priming
occurs. This is considered to be a phase that is necessary to trigger
the conscious process but does not generate the full conscious visual
state yet. The priming is done by a transient stimulus-evoked gamma
synchronization, encompassing primary sensory, higher sensory and
associative cortical areas, as described by Melloni et al. (2007);
c) Between 130-270 ms, a stimulus-evoked, feed-forward gamma
synchronous firing from sensory to associative areas occurs (see
single unit recordings, in visual areas of the anesthetized cat, by
Samonds and Bonds, 2005);
d) Around 270-300 ms, sparse responses to the visual stimulus occur in
higher associative areas (as registered by Quiroga et al., 2007),
which are related to the P3 component recorded by Del Cul et al.
(2007) and the P300 component referred by Melloni et al. (2007);
e) Beyond 300 ms, reentrant signaling from higher associative back to
sensory areas reach previously potentiated neuronal assemblies. From
this moment on, visual consciousness of the stimulus occurs. Gamma
oscillations, sustained with the participation of astrocytes in
glutamatergic tripartite synapses (Pereira and Furlan, 2007), become
phase-locked with alpha and theta (Palva and Palva, 2007), generating
brain-wide coherence of post-synaptic potentials.
As a conclusion, I recognize that brain correlates of visual
processing are more complex than previously thought. The picture that
emerges from the above synthesis of results is that correlates are not
reductible to a single event or type of event, but involve a complex
chain of distinct phases and mechanisms, as predicted in Arnold Trehub’s model of conscious visual
processing (Trehub, 1991).

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