As a working hypothesis we have assumed that only some types of specific neurons will express the NCC. It is already known (see the discussion under"Bistable Percepts") that the firing of many cortical cells does not correspond to what the animal is currently seeing. An alternative possibility is that the NCC is necessarily global (Greenfield, 1995). In one extreme form this would mean that, at one time or another, any neuron in cortex and associated structures could express the NCC. At this point, we feel it more fruitful to explore the simpler hypothesis -- that only particular types of neurons express the NCC -- before pursuing the more global hypothesis. It would be a pity to miss the simpler one if it were true. As a rough analogy, consider a typical mammalian cell. The way its complex behavior is controlled and influenced by its genes could be considered to be largely global, but its genetic instructions are localized, and coded in a relatively straightforward manner.
Where is the Visual Representation?
The conscious visual representation is likely to be distributed over more than one area of the cerebral cortex and possibly over certain subcortical structures as well. We have argued (Crick and Koch, 1995a) that in primates, contrary to most received opinion, it is not located in cortical area V1 (also called the striate cortex or area 17). Some of the experimental evidence in support of this hypothesis is outlined below. This is not to say that what goes on in V1 is not important, and indeed may be crucial, for most forms of vivid visual awareness. What we suggest is that the neural activity there is not directly correlated with what is seen.
We have also wondered (Crick, 1994) whether the visual representation is largely confined to certain neurons in the lower cortical layers (layers 5 and 6). This hypothesis is still very speculative.
What is Essential for Visual Consciousness?
The term "visual consciousness" almost certainly covers a variety of processes. When one is actually looking at a visual scene, the experience is very vivid. This should be contrasted with the much less vivid and less detailed visual images produced by trying to remember the same scene. (A vivid recollection is usually called a hallucination.) We are concerned here mainly with the normal vivid experience. (It is possible that our dimmer visual recollections are mainly due to the back pathways in the visual hierarchy acting on the random activity in the earlier stages of the system.)
Some form of very short-term memory seems almost essential for consciousness, but this memory may be very transient, lasting for only a fraction of a second. Edelman (1989) has used the striking phrase, "the remembered present," to make this point. The existence of iconic memory, as it is called, is well-established experimentally (Coltheart, 1983; Gegenfurtner and Sperling, 1993).
Psychophysical evidence for short-term memory (Potter, 1976; Subramaniam et al., 1997) suggests that if we do not pay attention to some part or aspect of the visual scene, our memory of it is very transient and can be overwritten (masked) by the following visual stimulus. This probably explains many of our fleeting memories when we drive a car over a familiar route. If we do pay attention (e.g., a child running in front of the car) our recollection of this can be longer lasting.
Our impression that at any moment we see all of a visual scene very clearly and in great detail is illusory, partly due to ever-present eye movements and partly due to our ability to use the scene itself as a readily available form of memory, since in most circumstances the scene usually changes rather little over a short span of time (O'Regan, 1992).
Although working memory (Baddeley, 1992; Goldman-Rakic, 1995) expands the time frame of consciousness, it is not obvious that it is essential for consciousness. It seems to us that working memory is a mechanism for bringing an item, or a small sequence of items, into vivid consciousness, by speech, or silent speech, for example. In a similar way, the episodic memory enabled by the hippocampal system (Zola-Morgan and Squire, 1993) is not essential for consciousness, though a person without it is severely handicapped.
Consciousness, then, is enriched by visual attention, though attention is not essential for visual consciousness to occur (Rock et al., 1992; Braun and Julesz, 1997). Attention is broadly of two types: bottom-up, caused by the sensory input; and top-down, produced by the planning parts of the brain. This is a complicated subject, and we will not try to summarize here all the experimental and theoretical work that has been done on it.
Visual attention can be directed to either a location in the visual field or to one or more (moving) objects (Kanwisher and Driver, 1992). The exact neural mechanisms that achieve this are still being debated. In order to interpret the visual input, the brain must arrive at a coalition of neurons whose firing represents the best interpretation of the visual scene, often in competition with other possible but less likely interpretations; and there is evidence that attentional mechanisms appear to bias this competition (Luck et al., 1997).
Recent Experimental Results
We shall not attempt to describe all the various experimental results of direct relevance to the search for the neuronal correlates of visual consciousness in detail but rather outline a few of them and point the reader to fuller accounts.
Action without seeing
Classical blindsight
This will already be familiar to most neuroscientists. It is discussed, along with other relevant topics, in an excellent book by Weiskrantz (1997). It occurs in humans (where it is rare) when there is extensive damage to cortical area V1 and has also been reproduced in monkeys (Cowey and Stoerig, 1995). In a typical case, the patient can indicate, well above chance level, the direction of movement of a spot of light over a certain range of speed, while denying that he sees anything at all. If the movement is less salient, his performance falls to chance; if more salient (that is, brighter or faster), he may report that he had some ill-defined visual percept, considerably different from the normal one. Other patients can distinguish large, simple shapes or colors. (For Weiskrantz's comments on Gazzaniga's criticisms, see pages 152-153; and on Zeki's criticisms, see pages 247-248.)
The pathways involved have not yet been established. The most likely one is from the superior colliculus to the pulvinar and from there to parts of visual cortex; several other known weak anatomical pathways from the retina and bypassing V1 are also possible. Recent functional magnetic resonance imaging of the blindsight patient G.Y. directly implicates the superior colliculus as being active specifically when G.Y. correctly discriminates the direction of motion of some stimulus without being aware of it at all (Sahraie et al., 1997 -- this paper should be consulted for further details of the areas involved).
The on-line system
The broad properties of the two hypothetical systems -- the on-line system and the seeing system -- are shown in Table I, following the account by Milner and Goodale in their book, The Visual Brain in Action (1995), to which the reader is referred for a more extended account. For a recent review, see Boussaoud et al., 1996. The on-line system may have multiple subsystems (e.g., for eye movements, for arm movements, for body posture adjustment, and so on). Normally, the two systems work in parallel, and indeed there is evidence that in some circumstances the seeing system can interfere with the on-line system (Rossetti, 1997).
One striking piece of evidence for an on-line system comes from studies on patient D.F. by Milner, Perrett and their colleagues (1991). Her brain has diffuse damage produced by carbon-monoxide poisoning. She is able to see color and texture very well but is very deficient in seeing orientation and form. In spite of this, she is very good at catching a ball. She can "post" her hand or a card into a slot without difficulty, though she could not report the slot's orientation.
It is obviously important to discover the difference between the on-line system, which is unconscious, from the seeing system, which is conscious. Milner and Goodale (1995) suggest that the on-line system mainly uses the dorsal visual stream. They propose that rather than being the "where" stream, as suggested by Ungerleider and Mishkin (1982), it is really the "how" stream. This might imply that all activity in the dorsal stream is unconscious. The ventral stream, on the other hand, they consider to be largely conscious. An alternative suggestion, due to Steven Wise (personal communication and Boussaoud et al., 1996), is that direct projections from parietal cortex into premotor areas are unconscious, whereas projections to them via prefrontal cortex are related to consciousness.
Our suspicion is that while these suggestions about two systems are on the right lines, they are probably over simple. The little that is known of the neuroanatomy would suggest that there are likely to be multiple cortical streams, with numerous anatomical connections between them (Distler et al., 1993). This is implied in Figure 1, a diagram often used by Fuster (Fuster, 1997: see his Fig. 8.4). In short, the neuroanatomy does not suggest that the sole pathway goes up to the highest levels of the visual system, and from there to the highest levels of the prefrontal system and then down to the motor output. There are numerous pathways from most intermediate levels of the visual system to intermediate frontal regions.
Figure 1: Fuster's figure (reproduced with permission by Lippincott-Raven Publishers) showing the fiber connections between cortical regions participating in the perception-action cycle. Empty rhomboids stand for intermediate areas or subareas of the labeled regions. Notice that there are connections between the two hierarchies at several levels, not just at the top level.
We would therefore like to suggest a general hypothesis:that the brain always tries to use the quickest appropriate pathway for the situation at hand. Exactly how this idea works out in detail remains to be discovered. Perhaps there is competition, and the fastest stream wins. The postulated on-line system would be the quickest of these hypothetical cortical streams. This would be the zombie part of you.
Bistable percepts
Perhaps the present most important experimental approach to finding the NCC is to study the behavior of single neurons in the monkey's brain when it is looking at something that produces a bistable percept. The visual input, apart from minor eye movements, is constant; but the subject's percept can take one of two alternative forms. This happens, for example, when one looks at a drawing of the well-known Necker cube.
It is not obvious where to look in the brain for the two alternative views of the Necker cube. Allman suggested a more practical alternative: to study the responses in the visual system during binocular rivalry (Myerson et al., 1981). If the visual input into each eye is differ
