How much of flavor perception is conscious and how much unconscious? Studies of smell are beginning to provide some intriguing answers. Traditionally, the neural basis of consciousness was ruled out as a subject for scientific study. However, recently it has become a growth industry in neuroscience. Leading the way have been a computational neuroscientist, Christof Koch, and his colleague Francis Crick. Crick, with James Watson, solved the structure of DNA in the early 1950s. He then turned his interest to neuroscience. Beginning in the 1970s, he took on the question of the neural basis of consciousness as a special interest, elevating it to one of the key problems that needed to be solved to understand the human brain and mind. Most neuroscientists, however, regarded it as an “ill-posed” question: consciousness was too vague a term to be the subject of scientific experiment. Most still think so.
Nonetheless, the two forged on. In a well-known synthesis in an article in 2003, Crick and Koch first define “consciousness” in a relatively narrow sense, only for the visual system, as “perceiving the specific color, shape or movement of an object.” They outline a framework in which primary sensory cortex at the “back” of the brain contains cells and microcircuits that act as “feature detectors” of the information relayed from the thalamus. Feature detection is believed to be largely unconscious. According to Crick and Koch, “The conscious mode for vision depends largely on the early visual areas (beyond V1) and especially on the ventral stream [in the temporal lobe].” This response is then relayed to the “front” of the brain, followed by complex backward and forward interactions between the prefrontal cortex and the visual association areas. One suggestion is that the forward connections are largely “driving” and the backward connections are largely “modulatory.” Consciousness, in this view, arises from special (as yet unspecified) firing properties of cortical neurons, in particular those that project from the sensory association areas to integrative (not primarily motor or sensory) areas of the prefrontal cortex.
No indication is given of how olfactory “conscious” perception would fit into this scenario. But smell and flavor raise many interesting questions about consciousness. In olfactory perception there is no “back” of the brain; the primary neocortical receptive area is in the orbitofrontal cortex, which is in the prefrontal area. Thus, in olfaction, all the sequences of processing necessary to get from the back to the front of the brain are compressed within the front of the brain itself. This reflects the evolutionary position of smell, with its privileged input to the highest centers of the frontal lobe throughout the evolution of the vertebrate brain. From this perspective, the best chance to reveal the neural basis of consciousness in mammals, including primates, should be sought in the olfactory system and its role in flavor.
“Is There Such a Thing as Blind Smell?”
These considerations were furthest from my mind a few years ago as I was getting ready to give a talk at the Society for Neuroscience on our first computer models of the interaction between an odor molecule and an olfactory receptor model, when Crick and Koch came in and took seats. I was elated with the prospect of having all that wisdom from the discovery of DNA applied now to how an odor molecule acts within the binding pocket of an olfactory receptor molecule. Sure enough, in the question period Francis rose, and I waited expectantly to hear his words of molecular wisdom: “Gordon,” he said (here it comes, I thought), “I wonder if you can tell me: Is there such a thing as blind smell?”
I was so surprised by this unexpected question that I could only sputter that I didn’t know, although I understood right away what he meant. He wanted to know if smell has something similar to a puzzling finding in vision called blind sight. This is demonstrated in patients who are legally blind from an injury to the visual cortex; if you show them pictures, they say they do not see anything. However, if they are forced to answer questions about them, the answers are above chance. It is as if they have rudimentary sight although they are blind; hence, “blind sight.” It indicates that without being conscious of it, their brains, containing a visual pathway rising only to the level of the thalamus, can actually register the visual scene.
Odors that we sniff but do not perceive? We never did resolve the question before Crick died several years ago. Of course, a pheromone in some ways qualifies as a “blind smell,” because it stimulates the olfactory pathway to bring about a behavioral response without the animal being conscious of it as a perception. Noam Sobel and his colleagues at the University of California, Berkeley, showed, using stimulation with a supposed human pheromone, that activation of fMRI signals in the brain occurred without awareness of stimulation by the subjects. But what Crick was interested in was not pheromones, but rather a situation in which a person has a brain injury that renders him or her unable to perceive smell stimuli consciously, yet can be shown to be able to perceive them unconsciously. The question goes to the heart of how conscious smell perception—and with it, flavor perception—arises in a pathway that does not go through the thalamus. There is now an answer. But first a little background.
Some Clues from the Smell Pathway
For a sensory stimulus to be perceived, we need to be conscious, alert, and paying attention. Understanding all these brain mechanisms would take us far beyond the main subject matter of neurogastronomy. However, the question of consciousness is relevant, because we cannot make use of our internal flavor image unless we are conscious. Thanks to Crick and Koch, the neural basis of consciousness is now a problem attracting some interest in neuroscience as well as in psychology and philosophy. Almost all the evidence and ideas relate to the visual system. The olfactory system has been almost entirely ignored. But, building on the facts we have covered, it may hold some interesting insights.
Where in the smell pathway does conscious perception of smell arise? Let us see if we can find any clues from what we have learned.
To review, the first smell station in the brain is the olfactory bulb, where the odor image is first formed and initial processing takes place. This processing is subject to the behavioral state of the animal through fibers originating deep within the brain. These fibers modulate processing of the odor image there depending on whether we are hungry or full (chapter 10). They also carry information about whether we are waking or sleeping, which is quite relevant to whether we are conscious or not, but it appears that this modulation occurs more centrally in the brain. We conclude that conscious perception of smell and of the spatial smell patterns does not arise in the olfactory bulb.
The next station is the olfactory cortex. Many regard this as the “primary” olfactory cortex, but, as discussed in chapter 12, in other sensory systems the term primary is reserved for the first area that the thalamus connects to in the neocortex. For example, in the visual pathway, conscious perception requires interactions between the thalamus and V1, its projection area in the occipital lobe at the back of the brain. Lack of V1 is what makes blind sight so paradoxical. It appears that there are a few thalamic fibers that project to surrounding association visual cortical areas to mediate this “unconscious” sight. Normally these surrounding areas elaborate the simple response in V1, but if they do not get their input from V1, conscious perception does not occur.
Regardless of whether conscious smell first arises in the olfactory cortex, the smell pathway, like all other sensory pathways, continues to the orbitofrontal cortex. I prefer to call this connection to the neocortex the primary olfactory cortex, with the use of primary similar to its use in the other sensory systems. In analogy with V1 in the visual system, it could be called “O1” in the olfactory system.
The connection to O1 of the orbitofrontal cortex is both direct and indirect (chapter 12). The larger direct projection is carried by the output axons of the pyramidal cells. These are the same axons that give rise to lateral inhibition within the olfactory cortex and the long re-excitatory association fibers that also carry centrifugal information back to the olfactory bulb. The smaller indirect projection is through activation, by the pyramidal cells, of cells in the endopiriform nucleus just deep to the pyriform cortex; their axons project to the mediodorsal thalamus, where they synapse with cells that also converge onto the olfactory orbitofrontal area.
Conscious Smell Perception
A big challenge is to understand the special nature of the direct projection that does not pass through the thalamus, a feature that makes the olfactory pathway unique among sensory systems. Surprisingly little attention has been given to this remarkable feature. The implications for conscious sensory perception should be one of the most intriguing challenges in cognitive neuroscience.
There are two possibilities. One is that conscious smell perception arises already at the level of the olfactory cortex. This idea is supported by the finding by Verity Brown in 2007 at the University of St. Andrews in Scotland that rodents in which the olfactory area of the orbitofrontal cortex has been removed can still perform normally on an odor identifcation task. If behaving rodents are regarded as “conscious,” this finding is significant for two reasons. First, it means that this is the only sensory pathway that gives rise to conscious sensory perception without reaching the neocortex and without engaging the thalamocortical system. Second, if this is so, we must ask: What are the subcortical mechanisms that replace the thalamus and the neocortex? In other sensory systems, the thalamus is involved in relaying brain stem activity that subserves “arousal” of the whole cortex when we are awake. In addition, Crick suggested many years ago that the thalamus also acts as a kind of attention “searchlight” to direct consciousness to the stimuli that need to be attended to. Because olfaction apparently does not have these mechanisms, how are the pathways for smell and for flavor coordinated with these thalamo-cortical mechanisms so that our perception appears to be conscious for smell in the same way as it is for the other systems?
These findings may apply particularly to rodents, because the same experiments in dogs produce profound deficits in the ability to smell. According to Noam Sobel and his colleagues, human subjects with trauma to the right thalamus show deficits in the ability to identify smells, and they also were found to experience less pleasantness of pleasant smells; this suggests that in humans the neocortical level is as necessary for smell perception as in other sensory systems, a finding that must generalize to flavor perception as well.
Answering Crick’s Question
This evidence in humans has received support from an unusual patient reported in 2010 by Jay Gottfried at Northwestern University. A 36-year-old patient named S. came to the hospital after suffering an injury to his head on the right side while falling down a flight of stairs. The injury caused bleeding into his right frontal lobe. His recovery proceeded well, except that he experienced a complete loss of his sense of smell, a condition called anosmia. A functional brain scan showed that he had damaged his right orbitofrontal cortex; other olfactory structures were not affected. Gottfried heard about the case and realized that it presented an unusual opportunity to test the role of the right orbitofrontal cortex in conscious smell, and brought S. to the laboratory for testing.
The subject’s psychological state was judged to be normal. Gottfried and his colleagues employed a standard method using Sniffin’ Sticks, small paddles coated with odor beads, to test (orthonasally) for smell perception. The test confirmed that S. was unable to detect any odor in either nostril, even at strong concentrations. The fact that the injury was only to the right orbitofrontal cortex supported the idea that most conscious processing of smell at the neocortical level occurs in the right orbitofrontal cortex. This kind of “lateralization” is unusual in sensory systems.
Even though S. was not conscious of the odors, he showed the ability to detect odors on the left side (the uninjured side) when tested against odorless controls. This meant that the left side smell pathway appeared normal whereas the right side was nonfunctional. Correlated with this, brain scans showed activity in the left olfactory pathway—the olfactory cortex and the orbitofrontal cortex—and the amygdala, often implicated in higher smell processing. The brain scans also showed activity in the right pathway up to the olfactory cortex, but none in the region of the damaged right orbitofrontal cortex. Finally, galvanic skin responses (the “lie detector” test) were used; they showed emotional responses to both right and left nostril stimulation—a further example of a response on the left side that was not consciously perceived.
Control experiments were carried out in normal uninjured subjects, which showed normal smell perception in both nostrils. The brain scans showed more activity in the right-sided smell pathway, supporting further the idea that smell processing tends to be lateralized to the right. It is interesting of course that the right side of the brain is believed to be the less logical and more artistic in its functions, which might be considered to be appropriate for elaboration perceptions of smell. The authors conclude that
[t]he fact that left-sided odor stimulation in Patient S. elicited appropriate peripheral and central responses suggests that the left olfactory system was largely preserved to support processing of the perceptual and emotional content of an odor, yet was unable to assign conscious awareness or feeling to that odor. Taken together, our data provide some of the first evidence to support the central role of the right OFC in facilitating the transformation of an upstream olfactory message into a conscious percept.
And what about Crick’s question? Gottfried and his colleagues conclude that “these findings reasonably satisfy criteria for the phenomenon of ‘blind smell.’” In support of the previous findings of Sobel and his colleagues, they observe:
An individual may be blind to (i.e., consciously unaware of) a smell, yet manifest reliable nonconscious responses to that smell. Of course, it is evident that Patient S. has lost more than mere olfactory awareness and exhibits only a rudimentary preservation of odor-detection ability…. However, the demonstration of odor-related activity in the left OFC… implies that the left olfactory pathway retains substantial functionality to implement olfactory sensory and affective analysis [that is unconscious to the subject].
In conclusion, this is a promising start to answering the question of where conscious perception of smell and flavor arise in the human brain flavor system, but we will need many more subjects and experiments like this to identify all the parts of the brain that contribute. With such a complex system, it is likely that conscious and unconscious perceptions will make their own contributions to the individual variations that make our flavor perceptions so fascinating.