You must remember this…

14 June 2013 by Malcolm Campbell, posted in Biology

The fundamental things apply…as time goes by" from As Time Goes By by Herman Hupfield (1894-1951)

Memory lurks. It lies in wait, biding time, waiting for an appropriate moment to reveal itself in its full glory.

We’ve all had that experience where our personal history seems to leap out of nowhere. Where past experience is laid out like a vast banquet – vivid in sight, smell, sound, touch and taste. While the memory is complex and rich, the trigger may be simple and subtle – the slightest of sounds, the most fleeting of glimpses, the faintest of whiffs.

For me, it was lilacs.

Lilacs are amongst the most fragrant of late spring blossoms. This deciduous, woody perennial grows as a small shrub or tree. It is widely planted as an ornamental in urban gardens, or as a hedgerow in more rural settings. In the late spring, it produces densely arranged tiny flowers. The beautiful little flowers, in shades of pink, mauve and lavender form clusters known as panicles.  When the late spring temperatures rise, these panicles release the characteristic lilac odour, an attractant for pollinators. This spring, this lilac odour triggered a memory like no other I have experienced before.

The memory harkens back to my years as a teenager.

As a teen, throughout the summer vacation, I worked on a farm. I started work there as soon as the school year ended, in the final days of spring. The work on the farm varied, but it always included repairing fences consisting of cedar rails. Some of these fences ran alongside a hedgerow of lilacs.

This spring, the scent of lilacs elicited the fullest of memory of that time. As my head filled with the aroma of lilac, my mouth recalled the bitter taste of iron nails clenched between teeth, mixed with the salty sweat from my upper lip. My right forearm and bicep flexed and fairly ached with the recollection of repetitive hammering. My left hand clenched at an invisible cedar rail that shed its imagined fibrous wood into my palm and under my fingernails. My eyes, or at least my mind’s eye, envisioned lush, swaying grass through brow-borne sweat. A warm summery breeze cut through the midday haze.

And my ears. My ears were filled with a soundtrack of the time – Fleetwood Mac’sDreams”, The Eagles’Hotel California” and “Life In The Fast Lane”, Stevie Wonder’sI Wish”, Alan O’Day’sUndercover Angel”, Stephen Bishop’sOn and On”, Steve Miller Band’sJet Airliner”, Manfred Mann Earth Band’sBlinded by the Light”, Hall and Oates’Rich Girl”, Jimmy Buffet’sMargaritaville” and so many more – all AM radio hits of a bygone era - embarrassingly unsophisticated, but an accurate reflection of the time and the place.

Altogether, it was like being thrown in a time machine and shot back the better part of 40 years. It was brief, but a wave of personal history washed over me. This said, it was no mere wave of nostalgia – a yearning for another time – but a palpable, intense complete reconstruction of another time. It was involuntary recollection, a rush of history that had emerged, seemingly, of its own doing.

Where did it come from?

The phenomenon I experienced has been described many times before, perhaps most famously, and certainly more lyrically, by Marcel Proust. Proust experienced what is known as autobiographical memory. As opposed to being triggered by an odour, Proust experienced his unbidden recollection upon eating a madeleine, a pastry from the region of France where Proust grew up. He describes the incident in À la recherche du temps perdu (In Search of Lost Time):

“No sooner had the warm liquid mixed with the crumbs touched my palate than a shiver ran through me and I stopped, intent upon the extraordinary thing that was happening to me. An exquisite pleasure had invaded my senses, something isolated, detached, with no suggestion of its origin. And at once the vicissitudes of life had become indifferent to me, its disaster innocuous, its brevity illusory…. I had ceased now to feel mediocre, contingent, mortal.

Proust recognised the involuntary nature of the recollection, the multitude of cues that could invoke the memory, and its qualitative distinction from what he called a voluntary memory:

“Voluntary memory, the memory of the intellect and the eyes, [gives] us only imprecise facsimiles of the past which no more resemble it than pictures by bad painters resemble the spring…. So we don’t believe that life is beautiful because we don’t recall it, but if we get a whiff of a long-forgotten smell we are suddenly intoxicated, and similarly we think we no longer love the dead, because we don’t remember them, but if by chance we come across an old glove we burst into tears.”

Proust’s description here is not only beautifully rendered, but also highly accurate. In the past decade, multiple studies have shown that odour-induced autobiographical memory is qualitatively different than voluntary memory. It is also deemed to be emotionally more intense than autobiographical memory induced by verbal or other auditory cues. In keeping with this, analyses of brain activity also support the notion that odour-induced autobiographical memories arise in the brain in a manner that is distinct from those that emerge from other stimuli.

This is all fine and well, but it still says nothing about the mechanism that invoked the involuntary autobiographical memory.

Evidence suggests that the there are two parts to the odour-based release of the memory. The first part is the perception of the odour. The second is the establishment and the release of the memory.

Odour perception, or olfaction, enables us to detect specific odorants. Odorants are detected by receptors, proteins that are embedded in the surface of olfactory neurons. Odorants are thought to bind to receptors via a model akin to a lock and key. The odorant, the key, fits within a particular lock, the receptor.

In the case of the lilac, the odorant is called terpineol. Terpineol is small molecule, comprising a mere 10 carbon atoms, 18 hydrogen atoms and one atom of oxygen. While small, terpineol has an elegant structure. Terpineol belongs to a class of compounds called monoterpene alcohol. Plants make many different monoterpenes, each with a distinct structure and, consequently, odour. The 10 carbon atoms in terpineol are arranged in a unique and intricate folding pattern. This comprises a six-carbon ring structure, with 4 carbons that dangle off the ring in a novel manner. There is a sole double bond, and an alcohol group (OH), both of which can migrate to some extent around the structure. This unique structure is what functions as the key that will fit into the odour receptor lock.

When the odorant docks with the receptor, the lock-and-key fit causes the receptor to initiate a signalling cascade, informing the cell – the  neuron – that the odorant has been detected. This detection signal is transmitted down the length of the sensory neuron to the olfactory bulb. The olfactory bulb then passes this information, via other neurons, to a several key regions of the brain, including, crucially, the amygdala. It is thought that the amygdala integrates the odour information, together with other sensory information, where is lays down a significant part of what will eventually be the autobiographical memory.

In the case of the formation of my autobiographical memory, the olfactory input was integrated with my other sensory experiences – the sights, sounds and tastes of the time – over days. These were stored in groups of interconnected neurons. Precisely how this memory is written and then recalled remains somewhat of a mystery, but it involves the control of gene function. What is a certainty though is that the transmission of this information involves signal transmission – the process of neurotransmission.

Neurotransmission is a remarkable process. Like olfaction, at the most fundamental level, neurotransmission involves the perception of small molecules, neurotransmitters, by receptor proteins. The major excitatory neurotransmitter, the one that is likely to be involved in conveying a signal when laying down autobiographical memory, is glutamate.

Glutamate is an interesting molecule. It plays multiple roles in our bodies. In addition to being a neurotransmitter, glutamate is one of the 20 essential amino acids that we use to build proteins. Glutamate also plays a central role in the movement of our body’s nitrogen into different metabolic pathways.

When it’s being used as a neurotransmitter, glutamate is released from an excited neuron so as to pass this excitation along to adjacent neurons. Glutamate is released at a specialised gap between neurons, the synapse. When glutamate is released by a neuron on one side of the synapse, it can be perceived by the neuron on the other side. This perception takes place through the activity of glutamate receptors, specialised proteins that bind to glutamate through the same sort of lock-and-key mechanism that odorant receptors used. There are different kinds of glutamate receptors, but one of the most important functions like a gate. When glutamate binds to this receptor, the glutamate “key” actually functions to unlock the gate, enabling ions to enter through the gate into the receptor neuron so as to excite it, and thereby convey excitation information from one neuron to the next.

The glutamate receptor that functions as a gate is an ancient mechanism. In fact, the glutamate-regulated gates predate the divergence of plants and animals. In plants these receptors also function to perceive glutamate, which induces them to open to let ions into the cell. This may seem a startling concept – plants don’t have a nervous system, so why would they possess a component of the neurotransmission system?

Plants use their glutamate receptors to monitor nutrient status. As plants are literally rooted in one place, they must monitor nutrients to make sure that allocation of metabolites to growth and development matches what is available to them. Glutamate turns out to be a very useful indicator of both carbon and nitrogen status in plants. Plant must ensure that there is an appropriate balance of carbon that has been integrated into metabolism via photosynthesis, versus organic nitrogen that has been taken up by the roots. Glutamate levels can help inform the plant if there is an excess of carbon relative to nitrogen, and vice versa. If there is an excess of carbon, it suggests that the plant is able to photosynthesise just fine, but that it needs to obtain more nitrogen from the soil.  Consequently, the plant would invest more of its resources in making roots relative to shoots and leaves. Conversely, if nitrogen is relatively high in comparison to carbon, the plant might scale back root growth in favour of making more shoots and leaves.

Glutamate helps plants monitor carbon and nitrogen and make “wise decisions” about resource allocation.

In some ways, glutamate functions to make a “memory” in plants, in that the investment in growth above or below the ground is a reflection of glutamate perception at different points in time.

Of course, this is not a memory as we think of it in humans, but it is a fixed imprint of a plant’s individual history, a “memory” of its past condition if you will.

This is an important consideration, as it points to how glutamate perception was undoubtedly used by the last common ancestor of plants and animals. A simple mechanism that was originally used to monitor nutritional status, remains in use for that purpose in plants. In fact, plants now have extended the use of their glutamate receptors, to perceive other amino acids. By contrast, animals have co-opted glutamate receptors for the purposes of forming entirely different kind of memories altogether – ones that are plastic, retrievable, utilisable.

It is this “utilisability” of memory that is undoubtedly the final source of my lilac-induced autobiographical experience. While modern living might make involuntary memory retrieval seem superfluous, it almost certainly served an important adaptive advantage in the relatively recent evolutionary innovation of our species. It is not difficult to imagine that an odour-induced memory that invokes all manner of sensory responses could have significant adaptive value.

As a means by which to prepare an individual for a series of coincident events, this kind of memory would be invaluable.

The scent of lilacs prepared me for everything I experienced in the hedgerow – what tastes and sounds to expect, what muscles would be brought to bear. Now, preparedness for hammering a cedar rails fence together while listening to 70s pop songs has little apparent value during a dog walk 40 years later in a city. However, an equivalent connection of events – such as the smell of lilacs coinciding with either capturing prey or avoiding being prey – would be pretty darn useful.

Given our relatively recent transition, on an evolutionary timescale, from a savannah-residing species to our “modern” domesticated selves, it should be no surprise that this circuitry remains intact. It wasn’t so long ago that it was incredibly useful.

And perhaps therein lies the utility of pondering such odour-induced memories today – they remind us of our connection to multiple scales of history.

There is the long term history of the glutamate receptors themselves – a mechanism that spans the aeons from the time that plants and animals were not yet separate lineages. A time when memory was imprinted in the growth and development of the organism.

Then there is the more recent evolutionary history. A time when unbidden memories might mean the difference between proper preparedness for getting a meal, or avoiding being a meal.

Finally there is our history as individuals within one lifespan. Here, involuntary memories shape our perception of our past, our present, and potentially our future.  Even today, there is the potential for adaptive value in “lilac-unlocked memory”. My experience was that it was invigorating – something that has been documented in previous studies, not to mention Proust’s prose. For a middle-aged person, it provided a wave of youthful feeling that I was able to ride for hours, if not days. If the exuberance I acquired from this can be translated into making life better for others, there may be some adaptive value in it yet. The old adage says to “Stop and smell the roses”. Perhaps “Stop and smell the lilacs” is more apt!

References:

Chu S & Downes JJ (2002) Proust nose best: Odors are better cues of autobiographical memory. Memory & Cognition 30: 511-518

Dietrich P et al. (2010) Physiology and biophysics of plant ligand‐gated ion channels. Plant Biology 12: 80-93

Forde BG & Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. Journal of Experimental Botany 58: 2339-2358

Gilliham M  et al. (2006) The Arabidopsis thaliana glutamate-like receptor family (AtGLR). In Communication in Plants (pp. 187-204). Springer Berlin Heidelberg.

Herz RS (2012) Odor memory and the special role of associative learning. Olfactory Cognition: From Perception and Memory to Environmental Odours and Neuroscience 85: 95-114

Tapken et al. (2013) A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids. Science Signaling 6: ra47

Troscianko ET (2013) Cognitive realism and memory in Proust’s madeleine episode. Memory Studies 1750698012468000

Willander J & Larsson M (2007) Olfaction and emotion: The case of autobiographical memory. Memory & Cognition 35: 1659-1663

Images: All photographs by Malcolm M. Campbell.

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