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.

References:

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