The Cinderella of the Senses: Smell as a Window into Mind and Brain?

Ann-Sophie Barwich — Visiting Assistant Professor in the Cognitive Science Program at Indiana University Bloomington

Smell is the Cinderella of our Senses. Traditionally dis­missed as com­mu­nic­at­ing merely sub­ject­ive feel­ings and bru­tish sen­sa­tions, the sense of smell nev­er attrac­ted crit­ic­al atten­tion in philo­sophy or sci­ence. The char­ac­ter­ist­ics of odor per­cep­tion and its neur­al basis are key to under­stand­ing the mind through the brain, however.

This claim might sound sur­pris­ing. Human olfac­tion acquired a rather poor repu­ta­tion through­out most of Western intel­lec­tu­al his­tory. “Of all the senses it is the one which appears to con­trib­ute least to the cog­ni­tions of the human mind,” com­men­ted the French philo­soph­er of the Enlightenment, Étienne Bonnot de Condillac, in 1754. Immanuel Kant (1798) even called smell “the most ungrate­ful” and “dis­pens­able” of the senses. Scientists were not more pos­it­ive in their judg­ment either. Olfaction, Charles Darwin con­cluded (1874), was “of extremely slight ser­vice” to man­kind. Further, state­ments about people who paid atten­tion to smell fre­quently mixed with pre­ju­dice about sex and race: Women, chil­dren, and non-white races — essen­tially all groups long excluded from the ration­al­ity of white men — were found to show increased olfact­ory sens­it­iv­ity (Classen et al. 1994). Olfaction, there­fore, did not appear to be a top­ic of reput­able aca­dem­ic invest­ment — until recently.

Scientific research on smell was cata­pul­ted into main­stream neur­os­cience almost overnight with the dis­cov­ery of the olfact­ory recept­or genes by Linda Buck and Richard Axel in 1991. It turned out that the olfact­ory recept­ors con­sti­tute the largest pro­tein gene fam­ily in most mam­mali­an gen­omes (except for dol­phins), exhib­it­ing a pleth­ora of prop­er­ties sig­ni­fic­ant for structure-function ana­lys­is of pro­tein beha­vi­or (Firestein 2001; Barwich 2015). Finally, the recept­or gene dis­cov­ery provided tar­geted access to probe odor sig­nal­ing in the brain (Mombaerts et al. 1996; Shepherd 2012). Excitement soon kicked in, and hopes rose high to crack the cod­ing prin­ciples of the olfact­ory sys­tem in no time. Because the olfact­ory path­way has a not­able char­ac­ter­ist­ic, one that Ramon y Cajal high­lighted as early as 1901/02: Olfactory sig­nals require only two syn­apses to go straight into the core cor­tex (form­ing almost imme­di­ate con­nec­tions with the amy­g­dala and hypo­thal­am­us)! To put this into per­spect­ive, in vis­ion two syn­apses won’t get you even out of the ret­ina. You can fol­low the rough tra­ject­ory of an olfact­ory sig­nal in Figure 1 below.

Three dec­ades later and the big rev­el­a­tion still is on hold. A lot of pre­ju­dice and neg­at­ive opin­ion about the human sense of smell have been debunked (Shepherd 2004; Barwich 2016; McGann 2017). But the olfact­ory brain remains a mys­tery to date. It appears to dif­fer markedly in its neur­al prin­ciples of sig­nal integ­ra­tion from vis­ion, audi­tion, and soma­to­sen­sa­tion (Barwich 2018; Chen et al. 2014). The back­ground to this insight is a remark­able piece of con­tem­por­ary his­tory of sci­ence. (Almost all act­ors key to the mod­ern molecu­lar devel­op­ment of research on olfac­tion are still alive and act­ively con­duct­ing research.)

Olfaction — unlike oth­er sens­ory sys­tems — does not main­tain a topo­graph­ic organ­iz­a­tion of stim­u­lus rep­res­ent­a­tion in its primary cor­tex (Stettler and Axel 2009; Sosulski et al. 2011). That’s neuralese for: We actu­ally do not know how the brain organ­izes olfact­ory inform­a­tion so that it can tell what kind of per­cep­tu­al object or odor image an incom­ing sig­nal encodes. You won’t find a map of stim­u­lus rep­res­ent­a­tion in the brain, such that chem­ic­al groups like ketones would sit next to alde­hydes or per­cep­tu­al cat­egor­ies like rose were right next to lav­ender. Instead, axons from the mitral cells in the olfact­ory bulb (the first neur­al sta­tion of olfact­ory pro­cessing at the front­al lobe of the brain) pro­ject to all kinds of areas in the piri­form cor­tex (the largest domain of the olfact­ory cor­tex, pre­vi­ously assumed to be involved in odor object form­a­tion). In place of a map, you find a mosa­ic (Figure 1).

What does this tell us about smell per­cep­tion and the brain in gen­er­al? Theories of per­cep­tion, in effect, always have been the­or­ies of vis­ion. Concepts ori­gin­ally derived from vis­ion were made fit to apply to what’s usu­ally side­lined as “the oth­er senses.” This tend­ency per­meates neur­os­cience as well as philo­sophy (Matthen 2005). However, it is a deeply prob­lem­at­ic strategy for two reas­ons. First, oth­er sens­ory mod­al­it­ies (smell, taste, and touch but also the hid­den senses of proprio­cep­tion and intero­cep­tion) do not res­on­ate entirely with the struc­ture of the visu­al sys­tem (Barwich 2014; Keller 2017; Smith 2017b). Second, we may have nar­rowed our invest­ig­at­ive lens and over­looked import­ant aspects also of the visu­al sys­tem that can be “redis­covered” if we took a closer look at smell and oth­er mod­al­it­ies. Insight into the com­plex­ity of cross-modal inter­ac­tions, espe­cially in food stud­ies, sug­gests that much already (Smith 2012; Spence and Piqueras-Fiszman 2014). So the real ques­tion we should ask is:

How would the­or­ies of per­cep­tion dif­fer if we exten­ded our per­spect­ive on the senses; in par­tic­u­lar, to include fea­tures of olfaction?

Two things stand out already. The first con­cerns the­or­ies of the brain, the oth­er the per­meable bor­der between pro­cesses of per­cep­tion and cognition.

First, when it comes to the prin­ciples of neur­al organ­iz­a­tion, not everything in vis­ion that appears crys­tal clear really is. The corner­stone of visu­al topo­graphy has been called into ques­tion more recently by the prom­in­ent neur­os­cient­ist Margaret Livingstone (who, not coin­cid­ent­ally, trained with David Hubel: one half of the fam­ous duo of Hubel and Wiesel (2004) whose find­ings led to the paradigm of neur­al topo­graphy in vis­ion research in the first place). Livingstone et al. (2017) found that the spa­tially dis­crete activ­a­tion pat­terns in the fusi­form face area of macaques were con­tin­gent upon exper­i­ence — both in their devel­op­ment and, inter­est­ingly, partly also their main­ten­ance. In oth­er words, learn­ing is more fun­da­ment­al to the arrange­ment of neur­al sig­nals in visu­al inform­a­tion pro­cessing and integ­ra­tion than pre­vi­ously thought. The spa­tially dis­crete pat­terns of the visu­al sys­tem may con­sti­tute more of a devel­op­ment­al byproduct than simply a genet­ic­ally pre­de­ter­mined Bauplan. From this per­spect­ive, fig­ur­ing out the con­nectiv­ity that under­pins non-topographic and asso­ci­at­ive neur­al sig­nal­ing, such as in olfac­tion, offers a com­ple­ment­ary mod­el to determ­ine the gen­er­al prin­ciples of brain organization.

Second, emphas­is on exper­i­ence and asso­ci­at­ive pro­cessing in per­cep­tu­al object form­a­tion (e.g., top-down effects in learn­ing) also mir­rors cur­rent trends in cog­nit­ive neur­os­cience. Smell has long been neg­lected from main­stream the­or­ies of per­cep­tion pre­cisely because of the char­ac­ter­ist­ic prop­er­ties that make it sub­ject to strong con­tex­tu­al and cog­nit­ive biases. Consider a wine taster, who exper­i­ences wine qual­ity dif­fer­ently by focus­ing on dis­tinct cri­ter­ia of obser­va­tion­al like­ness in com­par­is­on with a layper­son. She can point to subtle fla­vor notes that the layper­son may have missed but, after pay­ing atten­tion, is also able to per­ceive (e.g., a light oak note). Such influ­ence of atten­tion and learn­ing on per­cep­tion, ran­ging from nor­mal per­cep­tion to the acquis­i­tion of per­cep­tu­al expert­ise, is con­stitutive of odor and its phe­nomen­o­logy (Wilson and Stevenson 2006; Barwich 2017; Smith 2017a). Notably, the under­ly­ing biases (influ­enced by semant­ic know­ledge and famili­ar­ity) are increas­ingly stud­ied as con­stitutive determ­in­ants of brain pro­cesses in recent cog­nit­ive neur­os­cience; espe­cially in for­ward mod­els or mod­els of pre­dict­ive cod­ing where the brain is said to cope with the pleth­ora of sens­ory data by anti­cip­at­ing stim­u­lus reg­u­lar­it­ies on the basis of pri­or exper­i­ence (e.g., Friston 2010; Graziano 2015). While advoc­ates of these the­or­ies have centered their work on vis­ion, olfac­tion now serves as an excel­lent mod­el to fur­ther the premise of the brain as oper­at­ing on the basis of fore­cast­ing mech­an­isms (Barwich 2018); blur­ring the bound­ary between per­cep­tu­al and cog­nit­ive pro­cesses with the impli­cit hypo­thes­is that per­cep­tion is ulti­mately shaped by experience.

These are ongo­ing devel­op­ments. Unknown as yet is how the brain makes sense of scents. What is becom­ing increas­ingly clear is that the­or­iz­ing about the senses neces­sit­ates a mod­ern­ized per­spect­ive that admits oth­er mod­al­it­ies and their dimen­sions. We can­not explain the mul­ti­tude of per­cep­tu­al phe­nom­ena with vis­ion alone. To think oth­er­wise is not only hubris but sheer ignor­ance. Smell is less evid­ent in its con­cep­tu­al bor­ders and clas­si­fic­a­tion, its mech­an­isms of per­cep­tu­al con­stancy and vari­ation. It thus requires new philo­soph­ic­al think­ing, one that reex­am­ines tra­di­tion­al assump­tions about stim­u­lus rep­res­ent­a­tion and the con­cep­tu­al sep­ar­a­tion of per­cep­tion and judg­ment. However, a prop­er under­stand­ing of smell — espe­cially in its con­tex­tu­al sens­it­iv­ity to cog­nit­ive influ­ences — can­not suc­ceed without also tak­ing an in-depth look at its neur­al under­pin­nings. Differences in cod­ing, con­cern­ing both recept­or and neur­al levels of the sens­ory sys­tems, mat­ter to how incom­ing inform­a­tion is real­ized as per­cep­tu­al impres­sions in the mind, along with the ques­tion of what these per­cep­tions are and com­mu­nic­ate in the first place.

Olfaction is just one prom­in­ent example of how mis­lead­ing his­tor­ic intel­lec­tu­al pre­dilec­tions about human cog­ni­tion can be. Neuroscience fun­da­ment­ally opened up pos­sib­il­it­ies regard­ing its meth­ods and out­look, in par­tic­u­lar over the past two dec­ades. It is about time that we adjust our some­what older philo­soph­ic­al con­jec­tures of mind and brain accordingly.


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