Why do we experience such a rich visual world all of the time our eyes are open, but seem to be aware of smells only when they first occur? There do seem to be more than incidental and irrelevant differences between the olfactory system and the other four major sensory systems. Morsella et al. suggest that we study the olfactory system for clues as to the neural correlates of conscious perceptual content. However, the olfactory system is admittedly a very primitive, albeit highly conserved, sensory system. The olfactory cortex is paleocortex, only three layers deep. Moreover, as Morsella et al. emphasize, olfactory information does not pass through a thalamic “relay” nucleus on its way to the olfactory cortex, but rather goes directly there from the olfactory bulb, only informing the mediodorsal nucleus of the thalamus after paleocortical processing. Even that pathway is minor, as olfactory input is mainly directed to the orbitofrontal cortex, from where it also projects to the mediodorsal thalamus. Although some insights about consciousness can surely be gained by taking the olfactory system as a model, we believe that it is sufficiently different from the other sensory/perceptual systems that those insights will not be sufficient to explain much about the more sophisticated, and recently evolved, systems that subserve mammalian consciousness. Indeed, there might even be two separate types of consciousness: paleoconsciousness (paleoC), arising from a phylogenetically old system like the olfactory system, and neoconsciousness (neoC), arising from a more recent adaptation involving thalamic relay nuclei and extensive neocortical processing.
In the service of describing the newer type of consciousness, we offer the following observation: neoC has many properties that paleoC does not have. Most compelling to us is the fact that as long as we are awake and have our eyes open, we experience a rich visual scene. Conflict-resolving contents don't spring into and out of our consciousness, as described for Morsella et al.'s cave-dweller, although they do spring into and out of attention focus. Rather, we experience a wide range of action affordances; that is, following Gibson (e.g., Reference Gibson1979), Norman (e.g., Reference Norman2013), Turvey (e.g., Reference Turvey2015), and others, we experience action possibilities. The environment affords many such possibilities, the vast majority of which will not be relevant to current goals and plans, although they potentially could be. So why do we have perceptual and cognitive systems that afford such a huge set of possible actions, most of which will never be taken, conflict or no? Why did a simple system (paleoC), as described by Morsella et al., not suffice, in which relevant, conflict-resolving, perceptual content pops into consciousness when needed?
We contend that the more elaborate system (neoC) evolved, along with neocortex, to extend the range of affordances of animals in the service of niche construction (Withagen & van Wermeskerken Reference Withagen and van Wermeskerken2010). We suggest this is true at least for animals that appeared in the past several hundred million years, especially mammals and birds, which share most features of thalamocortical circuitry (Butler Reference Butler2008). Niche construction theory views affordances as coevolving along with the various species' physical characteristics to allow adaptive behavior in new niches that themselves are partially constructed from the new affordances available.
An especially important feature of the neoC system, which we contend does indeed involve essential thalamocortical circuitry, is that the affordances it provides allow for some very sophisticated behaviors. Many of these involve moving the entire body in complicated ways (e.g., a gymnast engaged in a floor routine). Another set enables us to extend our behaviors into nonlocal environments (cognitive maps; Tolman Reference Tolman1948) that allow for planning whole body movements to places beyond the range of direct perception (though see Stepp & Turvey [Reference Stepp and Turvey2015] and Turvey [Reference Turvey2015] for alternatives).
It should be noted that the behavior of Morsella et al.'s “creature in the cave” could arguably be construed as either conscious or non-conscious. For instance, the experience of “acting involuntarily” (e.g., suddenly reaching out to catch a falling object, the motions one's body takes to recover/brace during a fall, etc.) may only lack the illusion of voluntary action because the action is required to occur before its stimulus can reach consciousness (cf. Glover Reference Glover2004). Whether this issue can be resolved (re neoC/paleoC) may require further research, though determining “refresh rates” in other animals may prove fruitful.
Finally, we wish to point out that the paleoC and neoC systems, in advanced animals that have both, must work together to direct action. The olfactory system does project to neocortical areas, and those project their more advanced outputs to the mediodorsal thalamus, presumably integrating there with the information coming in directly from the piriform cortex. In addition, olfactory information entering the orbitofrontal cortex is integrated with information from every other sensory/perceptual system, and the integrated information is projected back to the sending areas, including the thalamus. It is therefore not surprising that understanding olfactory consciousness is difficult; the paleoC system does not normally function in isolation in advanced animals. When parts of the newer system to which it is connected are knocked out, however, as in damage to the mediodorsal thalamus or orbitofrontal cortex, anomalies of olfactory consciousness are experienced. One such anomaly is so-called blindsmell, in which a person denies olfactory experience but can make some olfactory discriminations. Notably, Sobel et al. (Reference Sobel, Prabhakaran, Hartley, Desmond, Glover, Sullivan and Gabrieli1999) observed increased activation levels of the orbitofrontal cortex and thalamus during high (compared with low, “non-perceptible”) concentrations of odorants. This phenomenon, and its brain correlates, closely resembles “blindsight,” “blindhearing,” and “blindtouch,” in all of which apparently unconscious information processing helps to guide action (Zucco et al. Reference Zucco, Priftis and Stevenson2014).
It is possible that our two suggested systems, paleoC and neoC, could share some fundamental mechanism that gives rise to experience. It is also possible that there is more than one such mechanism, with the more complicated one absorbing the less complicated, except when the more complicated one itself is incapacitated. Further exploration of the similarities and differences between olfactory consciousness and that illustrated by vision, hearing (especially speech), touch, and taste should continue to yield insight into this mystery.
Why do we experience such a rich visual world all of the time our eyes are open, but seem to be aware of smells only when they first occur? There do seem to be more than incidental and irrelevant differences between the olfactory system and the other four major sensory systems. Morsella et al. suggest that we study the olfactory system for clues as to the neural correlates of conscious perceptual content. However, the olfactory system is admittedly a very primitive, albeit highly conserved, sensory system. The olfactory cortex is paleocortex, only three layers deep. Moreover, as Morsella et al. emphasize, olfactory information does not pass through a thalamic “relay” nucleus on its way to the olfactory cortex, but rather goes directly there from the olfactory bulb, only informing the mediodorsal nucleus of the thalamus after paleocortical processing. Even that pathway is minor, as olfactory input is mainly directed to the orbitofrontal cortex, from where it also projects to the mediodorsal thalamus. Although some insights about consciousness can surely be gained by taking the olfactory system as a model, we believe that it is sufficiently different from the other sensory/perceptual systems that those insights will not be sufficient to explain much about the more sophisticated, and recently evolved, systems that subserve mammalian consciousness. Indeed, there might even be two separate types of consciousness: paleoconsciousness (paleoC), arising from a phylogenetically old system like the olfactory system, and neoconsciousness (neoC), arising from a more recent adaptation involving thalamic relay nuclei and extensive neocortical processing.
In the service of describing the newer type of consciousness, we offer the following observation: neoC has many properties that paleoC does not have. Most compelling to us is the fact that as long as we are awake and have our eyes open, we experience a rich visual scene. Conflict-resolving contents don't spring into and out of our consciousness, as described for Morsella et al.'s cave-dweller, although they do spring into and out of attention focus. Rather, we experience a wide range of action affordances; that is, following Gibson (e.g., Reference Gibson1979), Norman (e.g., Reference Norman2013), Turvey (e.g., Reference Turvey2015), and others, we experience action possibilities. The environment affords many such possibilities, the vast majority of which will not be relevant to current goals and plans, although they potentially could be. So why do we have perceptual and cognitive systems that afford such a huge set of possible actions, most of which will never be taken, conflict or no? Why did a simple system (paleoC), as described by Morsella et al., not suffice, in which relevant, conflict-resolving, perceptual content pops into consciousness when needed?
We contend that the more elaborate system (neoC) evolved, along with neocortex, to extend the range of affordances of animals in the service of niche construction (Withagen & van Wermeskerken Reference Withagen and van Wermeskerken2010). We suggest this is true at least for animals that appeared in the past several hundred million years, especially mammals and birds, which share most features of thalamocortical circuitry (Butler Reference Butler2008). Niche construction theory views affordances as coevolving along with the various species' physical characteristics to allow adaptive behavior in new niches that themselves are partially constructed from the new affordances available.
An especially important feature of the neoC system, which we contend does indeed involve essential thalamocortical circuitry, is that the affordances it provides allow for some very sophisticated behaviors. Many of these involve moving the entire body in complicated ways (e.g., a gymnast engaged in a floor routine). Another set enables us to extend our behaviors into nonlocal environments (cognitive maps; Tolman Reference Tolman1948) that allow for planning whole body movements to places beyond the range of direct perception (though see Stepp & Turvey [Reference Stepp and Turvey2015] and Turvey [Reference Turvey2015] for alternatives).
It should be noted that the behavior of Morsella et al.'s “creature in the cave” could arguably be construed as either conscious or non-conscious. For instance, the experience of “acting involuntarily” (e.g., suddenly reaching out to catch a falling object, the motions one's body takes to recover/brace during a fall, etc.) may only lack the illusion of voluntary action because the action is required to occur before its stimulus can reach consciousness (cf. Glover Reference Glover2004). Whether this issue can be resolved (re neoC/paleoC) may require further research, though determining “refresh rates” in other animals may prove fruitful.
Finally, we wish to point out that the paleoC and neoC systems, in advanced animals that have both, must work together to direct action. The olfactory system does project to neocortical areas, and those project their more advanced outputs to the mediodorsal thalamus, presumably integrating there with the information coming in directly from the piriform cortex. In addition, olfactory information entering the orbitofrontal cortex is integrated with information from every other sensory/perceptual system, and the integrated information is projected back to the sending areas, including the thalamus. It is therefore not surprising that understanding olfactory consciousness is difficult; the paleoC system does not normally function in isolation in advanced animals. When parts of the newer system to which it is connected are knocked out, however, as in damage to the mediodorsal thalamus or orbitofrontal cortex, anomalies of olfactory consciousness are experienced. One such anomaly is so-called blindsmell, in which a person denies olfactory experience but can make some olfactory discriminations. Notably, Sobel et al. (Reference Sobel, Prabhakaran, Hartley, Desmond, Glover, Sullivan and Gabrieli1999) observed increased activation levels of the orbitofrontal cortex and thalamus during high (compared with low, “non-perceptible”) concentrations of odorants. This phenomenon, and its brain correlates, closely resembles “blindsight,” “blindhearing,” and “blindtouch,” in all of which apparently unconscious information processing helps to guide action (Zucco et al. Reference Zucco, Priftis and Stevenson2014).
It is possible that our two suggested systems, paleoC and neoC, could share some fundamental mechanism that gives rise to experience. It is also possible that there is more than one such mechanism, with the more complicated one absorbing the less complicated, except when the more complicated one itself is incapacitated. Further exploration of the similarities and differences between olfactory consciousness and that illustrated by vision, hearing (especially speech), touch, and taste should continue to yield insight into this mystery.