In outlining a conceptual framework bearing on the organization and function of consciousness, Morsella et al. highlight the olfactory system as a test-bed and challenge for consciousness theory.

A trenchant comparison between olfaction and other senses has been provided by Köster (Reference Köster, Rouby, Schaal, Dubois, Gervais and Holley2002). For present purposes, olfaction stands out among our exteroceptive modalities in four principal respects:

1. 1. Its minimal “spatialization,” extending – in humans – to no more than a rudimentary left-right directionality, if any (Boireau et al. Reference Boireau, Pinault, Kirsche and MacLeod2000; Frasnelli et al. Reference Frasnelli, Charbonneau, Collignon and Lepore2009; Kobal et al. Reference Kobal, Van Toller and Hummel1989; Porter et al. Reference Porter, Anand, Johnson, Khan and Sobel2005).

2. 2. The ready, indeed profound, habituability of “ordinary odorants” (as noted by the authors and discussed in more detail below).

3. 3. Its heavy investment with innate odorant aversions and preferences (Khan et al. Reference Khan, Luk, Flinker, Aggarwal, Lapid, Haddad and Sobel2007; Kobayakawa et al. Reference Kobayakawa, Kobayakawa, Matsumoto, Oka, Imai, Ikawa, Okabe, Ikeda, Itohara, Kikusui, Mori and Sakano2007; Mandairon et al. Reference Mandairon, Poncelet and Bensafi2009; Mori & Sakano Reference Mori and Sakano2011; Nishizumi & Sakano Reference Nishizumi and Sakano2015; Yeshurun & Sobel Reference Yeshurun and Sobel2010).

4. 4. The extent to which some of its functions complete themselves without being represented in awareness, as in pheromonal signaling (Albrecht et al. Reference Albrecht, Demmel, Schöpf, Kleemann, Kopietz, May, Schreder, Zernecke, Brückmann and Wiesmann2011; Hummer & McClintock Reference Hummer and McClintock2009; Lundström & Olsson Reference Lundström and Olsson2005; Lundström et al. Reference Lundström, Boyle, Zatorre and Jones-Gotman2008; Mujica-Parodi et al. Reference Mujica-Parodi, Strey, Frederick, Savoy, Cox, Botanov, Tolkunov, Rubin and Weber2009; Saxton et al. Reference Saxton, Lyndon, Little and Roberts2008; Wyart et al. Reference Wyart, Webster, Chen, Wilson, McClary, Khan and Sobel2007; Zhou & Chen Reference Zhou and Chen2009; see also McClintock Reference McClintock, Wallen and Schneider2000; Wysocki & Preti Reference Wysocki and Preti2004).

Olfactory information that does enter or intrude on awareness does so in much the same way as information carried by other conscious modalities – namely, to lay claim on the deployment of our musculoskeletal resources for some instrumental purpose or other (Merker Reference Merker2007, p. 73; Morsella Reference Morsella2005). Thus, we arrive at the target article's “creature in the cave” example, or the jolt which, at the first faint whiff of burnt broccoli that reached my nostrils while engrossed in writing this commentary, sent me dashing to the kitchen to save my lunch from being turned to charcoal. The diamines cadaverine and putrescine on the one hand, and fruity esters on the other, exemplify odorants that make us steer our steps away from or towards natural sources of toxins or nutrients by filling our consciousness with unlearned powerful revulsion or more subtle attraction, respectively. Many an ordinary odorant does the same on the basis of learned associations, or acts simply as a novel or unexpected stimulus, eliciting the musculoskeletal orienting reflex (Sokolov Reference Sokolov1963) in search of its source.

In the absence of direct demands on the muskuloskeletal system, as in odorant effects on general propensities evidenced in mood, attitudes, or hormonal status, the operations of the olfactory system often proceed without awareness of the odorant itself (see references in the numbered list, point 4 above). The olfactory system thus offers natural opportunities for “contrastive analysis” (Baars Reference Baars, Flanagan, Block and Guzeldere1997a) by tracing differential information flow in cases of subliminal versus conscious olfaction. This is all the more so because the olfactory bulb in humans, who apparently lack a functional vomeronasal organ (Mast & Samuelsen Reference Mast and Samuelsen2009; Savic et al. Reference Savic, Hedén-Blomqvist and Berglund2009), carries both pheromonal and ordinary odor information to the brain (Mori & Sakano Reference Mori and Sakano2011; see also Friedrich Reference Friedrich2011).

In attentional terms, conscious olfaction behaves like other sensory modalities at least to the extent that attention to olfaction facilitates odor detection. This facilitation takes place in the presence of increased functional connectivity along the “indirect pathway” from piriform to orbitofrontal cortex via the mediodorsal nucleus of the thalamus (Plailly et al. Reference Plailly, Howard, Gitelman and Gottfried2008). The lack of olfactory “spatialization” makes attention of the directional kind largely irrelevant to olfaction (Sela & Sobel Reference Sela and Sobel2010).

There is, however, a particular attentional effect that could in principle be shared with the other senses but appears to be altogether lacking in olfaction. In other exteroceptive modalities, information that has disappeared from awareness on account of habituation (say, the humming of a refrigerator, or the touch of one's clothing on the body) can be restored to awareness by an act of deliberate attention. Not so for olfaction (Köster Reference Köster1971; Reference Köster, Rouby, Schaal, Dubois, Gervais and Holley2002; Stevenson Reference Stevenson2009). There is simply no way to restore the habituated smell of one's home to awareness by attentional effort. Typically, its characteristic smell is detectable only after returning home from a prolonged absence. This is the profound habituability of ordinary odors (as opposed to some “extraordinary” ones: try habituating to the smell of cadaverine!) mentioned in point 2 above.

This unavailability of ordinary odorants to deliberate dishabituation is a direct consequence, I suggest, of the fact that the “deliberately dishabituable” modalities enter the telencephalon via a first-order thalamic relay. Olfaction, on the other hand, enters directly, by making its first central synapses in allocortical prefrontal and immediately adjoining medial temporal areas without first having passed through the thalamus (Carmichael et al. Reference Carmichael, Clugnet and Price1994). This places olfaction outside the umbrella of the mechanism by which cortical layer VI pyramidal cells “tune” information on its “way up” to the cortex from first-order nuclei (for which see Merker 2013c, p. 2), an arrangement that may allow deliberate dishabituation of the affected modalities to take place. To the best of my knowledge, this is the first time this anatomical arrangement is proposed to bear on dishabituability and its lack in olfaction, a conjecture which this commentary allows me to commit to print.

How, then, does olfactory information become conscious, when it does? That, of course, depends upon what your “paradigm of consciousness” dictates regarding the necessary and sufficient conditions for information to attain conscious status. In a series of previous publications, I have elaborated one such paradigm (Merker Reference Merker2007, Reference Merker, Shimon, Tomer and Zach2012; Reference Merker, Pereira and Lehmann2013a; 2013c). It proposes that cortical operations, cast in probabilistic form, would benefit from having final estimates precipitated extra-cortically, in a subcortical “global best estimate buffer,” for purposes of optimizing moment-to-moment serial behavior. The nested format of this buffer renders its contents conscious. I have conjecturally assigned this multimodal buffer to a region of unique connectivity in the dorsal pulvinar, where unit activity shows more selectivity for stimulus awareness than cortical visual areas assessed with the same flash-suppression method (see Wilke et al. Reference Wilke, Mueller and Leopold2009).

From this perspective, the irreducible requirement for olfactory stimuli to reach awareness is that olfactory information reach this pulvinar territory. Does it? The short answer would seem to be yes, and rather directly at that. In the monkey, the olfactory bulb itself projects to at least eight separate telencephalic territories. One of these is the anterior entorhinal cortex (Carmichael et al. Reference Carmichael, Clugnet and Price1994). Entorhinal cortex in turn is reciprocally connected with the relevant portions of the pulvinar (Insausti et al. Reference Insausti, Amaral and Cowan1987; Saunders et al. Reference Saunders, Mishkin and Aggleton2005). From this perspective at least, olfactory anatomy does not pose any insuperable obstacles to consciousness theory. I thank Ezequiel Morsella and colleagues for providing an opportunity to make these remarks on conscious olfaction.