Smell-locked memories: our infancy in odours

The sense of smell emerges very early in human foetal development; and, research shows that the association of odours with learning begins very early in life while we are still in our mother’s womb 1,2. In fact, to some extent it was shown that if we appreciate a certain smell or not soon after we are born, it much depends on whether our mothers ingested that specific fragrant food during the pregnancy or not 1.

Furthermore, studies suggest that human olfaction is unique in its ability to cue the emotional aspects of autobiographical memory, including experiences formed early in life3 – the so-called Proust phenomenon. In “Swann’s Way”, the first volume of “À la recherche du temps perdu”, Marcel Proust as a nostalgic incident of involuntary memory, which is recalled by dipping madeleines in lime-flower tea when sitting next to its aunt Léonie before going to church on Sunday mornings in Combray. 

Such odour memories can convey an intense vivid visceral sense of the past, as if it was being re-experienced 4; with odour-cued memories described as more vivid than memories evoked by corresponding words or pictures 5. Specifically, most odour-cued memories are locked in the first decade of our lives (<10 years), whereas memories associated with verbal and visual cues seem to peak during early adulthood (11–20 years) 2,6. Also, odour-evoked memories were shown to be rarer and less frequently thought about 7.

The reason for such exceptionally visceral and vivid experience when recalling such memories relates to the fact that the olfaction has a privileged and unique connection to the neural anatomic substrates of emotion and associative-learning. In our brain, the primary olfactory cortex includes the amygdala – which processes emotional experience and emotional memory; as well as the hippocampus, which is involved in associative-learning 4. As such, just the act of smelling immediately activates the amygdala-hippocampal complex. Furthermore, while we are recollecting an odour-evoked memory, the amygdala is more activated than when we smell similar odours that do not evoke a memory 8. Additionally, the second olfactory cortex (orbitofrontal cortex) specifically assigns an affective value to that stimulus, that specific odour, and determines a reinforcement value – none of our other senses does that 4,5,8.

Not only pleasant memories can be triggered, but odours are especially effective at triggering fearful or traumatic memories that help us be aware of future danger. Recently, Hakim and colleagues from Queensland University of Technology of Brisbane, Australia, have shown that in mice, by testing olfactory fear memory recall after 24h, they could see behavioural and cellular changes of long-term reconsolidated memory that could return to a labile state after 14 days 9. This organic malleability seen by an increased density of pCREB- (phosphorylated cyclic adenosine monophosphate response element binding protein) and pMAK- (phosphorylated mitogen-activated protein kinase) -positive immunoreactive neurons in the medial/cortical subnuclei of the amygdala and the posterior piriform cortex of mice, might allow one day for us to manipulate such reactivating fear memories and create conditions to prevent reconsolidation – avoiding that such fears and traumas could hunt us again.

In a simplistic sense, like other animals of the natural kingdom which are guided by their highly conserved olfactory sensory system in their daily lives, our memories can also be smell-locked inside to guide us through life. 

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References

1          Schaal, B., Marlier, L. & Soussignan, R. Human foetuses learn odours from their pregnant mother’s diet. Chem Senses 25, 729-737 (2000). https://doi.org:10.1093/chemse/25.6.729

2          Mouly AM, S. R. Memory and Plasticity in the Olfactory System: From Infancy to Adulthood Vol. Chapter 15 (CRC Press/Taylor & Francis, 2010).

3          Chu, S. & Downes, J. J. Proust nose best: odors are better cues of autobiographical memory. Mem Cognit 30, 511-518 (2002). https://doi.org:10.3758/bf03194952

4          Herz, R. S. The Role of Odor-Evoked Memory in Psychological and Physiological Health. Brain Sci 6 (2016). https://doi.org:10.3390/brainsci6030022

5          Herz, R. S. & Schooler, J. W. A naturalistic study of autobiographical memories evoked by olfactory and visual cues: testing the Proustian hypothesis. Am J Psychol 115, 21-32 (2002). 

6          Willander, J. & Larsson, M. Smell your way back to childhood: autobiographical odor memory. Psychon Bull Rev 13, 240-244 (2006). https://doi.org:10.3758/bf03193837

7          Miles, A. N. & Berntsen, D. Odour-induced mental time travel into the past and future: do odour cues retain a unique link to our distant past? Memory 19, 930-940 (2011). https://doi.org:10.1080/09658211.2011.613847

8          Herz, R. S., Eliassen, J., Beland, S. & Souza, T. Neuroimaging evidence for the emotional potency of odor-evoked memory. Neuropsychologia 42, 371-378 (2004). https://doi.org:10.1016/j.neuropsychologia.2003.08.009

9          Hakim, M. et al. Retrieval of olfactory fear memory alters cell proliferation and expression of pCREB and pMAPK in the corticomedial amygdala and piriform cortex. Chemical Senses 47 (2022). https://doi.org:10.1093/chemse/bjac021