What counts as "memory" and who gets to define it?

Do Plants Have “Memory”?

A new paper by Bédécarrats et al. (2018) is the latest entry into the iconoclastic hullabaloo claiming a non-synaptic basis for learning and memory. In short, “RNA extracted from the central nervous system of Aplysia given long-term sensitization training induced sensitization when injected into untrained animals...” The results support the minority view that long-term memory is not encoded by synaptic strength, according to the authors, but instead by molecules inside cells (à la Randy Gallistel).

Adam Calhoun has a nice summary of the paper at Neuroecology:

...there is a particular reflex ¹ (memory) that changes when they [Aplysia] have experienced a lot of shocks. How memory is encoded is a bit debated but one strongly-supported mechanism (especially in these snails) is that there are changes in the amount of particular proteins that are expressed in some neurons. These proteins might make more of one channel or receptor that makes it more or less likely to respond to signals from other neurons. So for instance, when a snail receives its first shock a neuron responds and it withdraws its gills. Over time, each shock builds up more proteins that make the neuron respond more and more. These proteins are built up by the amount of RNA (the “blueprint” for the proteins, if you will) that are located in the vicinity of the neuron that can receive this information.  ...

This new paper shows that in these snails, you can just dump the RNA on these neurons from someone else and the RNA has already encoded something about the type of protein it will produce.

Neuroskeptic has a more contentious take on the study, casting doubt on the notion that sensitization of a simple reflex to any noxious stimulus (a form of non-associative “learning”) produces “memories” as we typically think of them. But senior author Dr. David Glanzman tolerated none of this, and expressed strong disagreement in the comments:

“I’m afraid you have a fundamental misconception of what memory is. We claim that our experiments demonstrate transfer of the memory—or essential components of the memory—for sensitization. Now, although sensitization may not comport with the common notion of memory—it’s not like the memory of my Midwestern grandmother’s superb blueberry pies, for example—it nevertheless has unambiguous status as memory.  ...  [didactic lesson continues] ...  We do not claim in our paper that declarative memories—such as my memory of my grandmother’s blueberry pies—or even simpler forms of associative memories like those induced during classical conditioning—can be transferred by RNA. That remains to be seen.”

OK, so Glanzman gets to define what memory is. But later on he's caught in a trap and has to admit:

“Of course, there are many phenomena that can be loosely regarded as memory—the crease in folded paper, for example, can be said to represent the memory of a physical action.”

That was in response to Harvey-6-3.5, who said:

“So a transfer of RNA that activates a cellular mechanism associated with touch isn't memory, but rather just exogenously turning on a cellular pathway. By that logic, gene therapy to treat sickle cell anemia changes blood "memory".” ²

However, my favorite comment was from Smut Clyde:

“Kandel set the precedent that reflexes in Aplysia are "memories", and now we're stuck with it.”

This reminded me of Dr. Kandel's bold [outlandish?] attempt to link psychoanalysis, Aplysia withdrawal reflexes, and human anxiety (Kandel, 1983). I was a bit flabbergasted that gill withdrawal in a sea slug was considered “mentation” (thought) and could support Freudian views.³

In the past, ascribing a particular behavioral feature to an unobservable mental process essentially excluded the problem from direct biological study because the complexity of the brain posed a barrier to any complementary biological analysis. But the nervous systems of invertebrates are quite accessible to a cellular analysis of behavior, including certain internal representations of environmental experiences that can now be explored in detail; This encourages the belief that elements of cognitive mentation relevant to humans and related to psychoanalytic theory can be explored directly [in Aplysia] and need no longer be merely inferred.

- click on image for a larger view -

So anticipatory anxiety in humans is isomorphic to invertebrate responses in a classical aversive conditioning paradigm, and chronic anxiety is recreated by long-term sensitization paradigms. Perhaps I missed the translational advances here, and any application to Psychoanalytic and Neuropsychoanalytic practice that has been fully realized.

If we want to accept a flexible definition of learning and memory in animals, why not consider associative learning experiments in pea plants, where a neutral cue predicting the location of a light source had a greater effect on the direction of plant growth than innate phototropism (Gagliano et al., 2016)? Or review the literature on associative and non-associative learning in Mimosa? (Abramson & Chicas-Mosier, 2016). Or evaluate the field of ‘plant neurobiology’ and even the ‘Philosophy of Plant Neurobiology’ (Calvo, 2016). Or are the possibilities of chloroplast-based consciousness and “mentation” without neurons too threatening (or too fringe)?

But in the end, we know we've reached peak plant cognition when a predictive coding model appears — Predicting green: really radical (plant) predictive processing (Calvo & Friston, 2017).


Further Reading

The Big Ideas in Cognitive Neuroscience, Explained (especially the sections on Gallistel and Ryan)

What are the Big Ideas in Cognitive Neuroscience? (you can watch the videos of their 2017 CNS talks)


Footnotes

¹ edited to indicate my emphasis on reflex — more specifically, the gill withdrawal reflex in Aplysia — which can only go so far as a model of other forms of memory, in my view.

²  Another skeptic (but for different reasons) is Dr. Tomás Ryan, who was paraphrased in Scientific American:

But [Ryan] doesn’t think the behavior of the snails, or the cells, proves that RNA is transferring memories. He said he doesn’t understand how RNA, which works on a time scale of minutes to hours, could be causing memory recall that is almost instantaneous, or how RNA could connect numerous parts of the brain, like the auditory and visual systems, that are involved in more complex memories.

³ But I haven't won the Nobel Prize, so what do I know?


References

Abramson CI, Chicas-Mosier AM. (2016). Learning in plants: lessons from Mimosa pudica. Frontiers in psychology Mar 31;7:417.

Bédécarrats A, Chen S, Pearce K, Cai D, Glanzman DL. (2018). RNA from Trained Aplysia Can Induce an Epigenetic Engram for Long-Term Sensitization in Untrained Aplysia. eNeuro. May 14:ENEURO-0038.

Calvo P. (2016). The philosophy of plant neurobiology: a manifesto. Synthese 193(5):1323-43.

Calvo P, Friston K. Predicting green: really radical (plant) predictive processing. Journal of The Royal Society Interface. 14(131):20170096.

Gagliano M, Vyazovskiy VV, Borbély AA, Grimonprez M, Depczynski M. (2016). Learning by association in plants. Scientific Reports Dec 2;6:38427.

Kandel ER. (1983). From metapsychology to molecular biology: explorations into the nature of anxiety. Am J Psychiatry 140(10):1277-93.