February 11

Through the Nostril Gates to the Past

[En Español]

My very first childhood memory, as much as I can tell, is one of sour feet. It happened during one of the mandatory nap sessions in kindergarten, where everyone slept on little mats barely above the floor. Being inexplicably awake on my side, unaware of the caretaker’s silent patrol behind me, I made a turn—trying to get comfortable, no doubt—and was hit right in my nose by a rancid wave of such foul odor that, even to this day, the occasional bold wafts of certain cheeses in grocery stores can still give me revolting glimpses of the skin-colored stockings and their noxious content.

Of course, I am not alone in acknowledging the far-reaching power of scents to bring back the past; according to a 1987 survey in the U.S. by National Geographic, out of ~26,000 respondents, across all age groups (from 20s to 80s), at least 30% reported at least one vivid memory elicited by one of the six odors provided [1]. More recently, reputable entertainment venues such as Mashable and BuzzFeed have compiled lists upon lists of nostalgia-inducing smells, from Play-Doh to candy floss. My own anecdote is but one example of the so-called “Proust Effect/Phenomenon”. Named after a brilliant, if verbose, French writer who was often in search of lost time, the Proust phenomenon describes the ability to write long-winded introductory paragraphs of odors to cue autobiographical memories that are old, vivid, and emotionally charged [2].

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A scene of smell/taste-induced involuntary memory, i.e. a fine example of the Proust phenomenon, from the animated Pixar film Ratatouille.

But why is the Proust phenomenon, colloquially speaking, a thing? If the sense of smell, or olfaction, truly has some unique properties that makes it a shortcut to forming emotionally labeled salient memories, then why do we have this shortcut to begin with? After all, psychologists have reported since the 70s that vision, not olfaction, is our dominant sense [3]. Not to mention that, as I spent more than a year in the same kindergarten, I must have had encounters with the breathtaking caretaker more than once, yet I (thankfully) remember only one such event. If the olfactory-autobiographical shortcut exists, why does it seem to be active only occasionally? To answer these questions fully requires verbiage and verbosity I cannot afford, but I will make an attempt to sketch the neurobiological underpinnings of these curious observations.

Olfaction, at its very basic level, can be described as “knowing what kind of chemical compounds are in the air”. For our ancient bacterial relatives that swam in primordial soups, there were only two broadly categorized senses: chemo-sense, i.e. “old-fashioned olfaction”, and mechano-sense, i.e. “touch” [4]. Of these two, chemo-sense was the dominant source of information; a great multitude of protein machineries suitable to catch different molecules—or “odorants”, for bigger animals with a sense of smell—were developed over the ages, whereby bacteria could move towards nutritious sugary compounds and away from potentially harmful ones [4]. This advantageous scheme, where chemical signal receptors along the cell-world boundary pick up environmental cues relevant to one’s survival, has been preserved by evolution in many different forms to this day, with everything between forage and procreation benefitting from it [5].

In mammals like ourselves, the implementation of this scheme has the nose as a prominent characteristic. The nose offers moderate protection for our olfactory epithelium, a layer of tissue that contains neurons capable of identifying airborne chemical compounds, while providing access to fragrant rose, pungent wine, and stinky foot via inhaled air. While we do not depend nearly as much on olfaction as dogs or rats —the mammalian champions of odor identification—in daily life, and recognize only a small fraction of odors available to our furry cousins [6], we do still have a dedicated part of our nervous system with similar circuitry. The olfactory epithelium neurons communicate via the olfactory nerve to the olfactory bulbs, neural structures that relay information to the cerebral cortex where, as far as we know, autobiographical memories form [7]. Like the chemo-sense of bacteria (or any sense, really), mammalian olfaction is primarily concerned with survival, an observation that lends itself well to the bulb-to-cortex architecture of our olfactory apparatus: direct connections exist between the olfactory bulb and piriform/olfactory cortex on two crucial structures involved in emotion and memory: the amygdala and hippocampus [7]. This architecture, in short, is quite possibly part of the “shortcut” I mentioned earlier.

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A simplified diagram of the mammalian olfactory system. OSN: olfactory sensory neuron.

The power of this olfactory shortcut, then, likely derives from the power of emotion in “binding” events to long-term memory. This binding process, in mammals, has been proposed to rely on the amygdala, and enhances emotional memory over time [8]. In humans, several case studies showed that damage to both amygdalae (we each have two) either eliminates or severely reduces this enhancement of episodic memory—a category that includes autobiographical memory—containing emotional (e.g. gruesome scene of horror movie) materials, but does not change memory recall performance for neutral (e.g. closing credits of horror movie) materials [8]. The actual “memorizing”, in turn, depends on the interaction between the hippocampus and the rest of the cerebral cortex [9]. I think it is reasonable to expect that, with olfactory information carried readily and more or less simultaneously to both amygdala and hippocampus [7], the sense of smell is in a prime position to generate strong memories that persist over time, which would have provided substantial survival perks to, say, a rat that lived in the urine-littered hunting range of wild cats.

Taking the rat hypothetical and running with it, one might notice that it certainly would be to the rat’s advantage if, say, the rat remembered every trace of urine after the first encounters—a forgetful second visit just might prove fatal, after all. Meanwhile, being scared by every waft of odor, old or new, might just be too exhausting a way to live. What seems to be needed is a novelty-detection system that strongly “rewards” the first encounters and produce a lasting memory, and also renders said memory relatively stable. Indeed, there is evidence in mice that novelty of the environmental odors determines the effects of olfactory enrichment on memory by making the olfactory bulb more malleable to change, through the regulatory molecule norepinephrine [10]. The olfactory bulb is also one of the only two places in most mammalian brains to support adult neurogenesis, where new neurons can be found throughout adulthood, despite the common wisdom that neurons are more or less for life, and experiences with novel odors indeed led to apparent increases in olfactory bulb tissue concentration in mice [10]. Given the reciprocal connections between the olfactory bulb and the hippocampus via the entorhinal cortex, another key area in episodic memory formation [7], I am willing to bet a not insignificant sum that monitoring both the olfactory bulb and the hippocampus simultaneously would help clarify the nature of our Proustian shortcut even further.

While we now know quite a bit about how an olfactory memory might be expediently formed, there are still more mysteries to be examined: can a good smell “overwrite” the bad, if the sensory context remains the same otherwise? Why do we seem to only remember a small fraction, even among the memories accompanied by odors that produce strong opinions? Do chefs, perhaps, have better memories about their own lives? If such musings pique your interest, dear reader, be assured that you are not alone in your curiosity. And as much as this post has been about the past, I believe that it is time now to look forward, instead, to the future, whatever smells it may bring.

 

References:

[1] Gilbert, A. N., Wysocki, C. J. The smell survey results. Natl. Geographic 172:514-525 (1987).

[2] Chu, S., Downes, J. J. Odour-evoked autobiographical memories: psychological investigations of Proustian phenomena. Chem. Senses 25 (1): 111-116 (2000).

[3] Posner, M. I., Nissen, M. J.,  Klein, R. M. Visual dominance: an information-processing account of its origins and significance. Psychol. Rev. 83 (2): 157-171 (1976).

[4] Harapanahalli, A. K. et al., Chemical signals and mechanosensing in bacterial responses to their environment. PLoS Pathog. 11 (8):  e1005057 (2015).

[5] Stocker, R. F., Olfactory coding: connecting odorant receptor expression and behavior in the drosophila larva. Curr. Biol. 16 (1): R16-R18 (2006).

[6] Quignon, P. et al., The dog and rat olfactory receptor repertoires. Genome Biol. 6 (10): R83

[7] Mouly, A., Sullivan, R. Memory and plasticity in the olfactory system: from infancy to adulthood. The Neurobiology of Olfaction Ch. 15, CRC Press/Taylor & Francis (2010).

[8] Yonelinas, A. P., Ritchey, M. The slow forgetting of emotional episodic memories: an emotional binding account. Trends Cogn. Sci. 19 (5): 259-267 (2015).

[9] Nadel, L., Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7: 217-227 (1997).

[10] Veyrac, A. et al., Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 34: 786-795 (2009).

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