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Hippocampus without a hippocampus

13/2/2017

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Hippocampus
A Black-sea seahorse (Hippocampus hippocampus). Photo by Florin Dumitrescu (from Wikimedia)
My last post was all about fish memory. However, there is more than one type of memory. For example, you have “working” memory which you use when you’re at the bar to remember someone’s phone number from the time they give it to you until you can find a napkin to write it on. This kind of memory has a limited capacity of about 7 items (which is why phone numbers are only 7 digits long) and can easily be disrupted. If, while frantically searching for a napkin and pen, some drunk friend asks you how much tip they should leave, that might be enough to knock the phone number out of your working memory. You also have a “reference” memory, which is where you keep things we remember for longer, like your own phone number. Reference memory doesn’t seem to have capacity limits. Back before we outsourced our memory to our phones, people used to memorize large chunks of Shakespeare and the Bible and nobody ever complained of their memory being full.

Memory can be sliced even finer than that. One distinction, first made in the 1970’s by Endel Tulving [1], is between “episodic” and “semantic” memory, both subtypes of reference memory. Semantic memory is your memory for facts about the world, for example, that the sun rises in the morning. Episodic memory is for specific events in your own life, like remembering watching the sunrise yesterday (while pining over that lost phone number). Episodic memories are distinguished by being full of details: you recall where the event took place, how long ago, what you were wearing, and why it clashed with your handbag. Knowing your own phone number is a sematic memory; remembering the day you bought your new phone and got that number is episodic.

By studying people who had suffered accidents that damaged their brains, researchers have found that different kinds of memory live in different parts of the brain. Episodic memory, in humans, seems to live in a part of the brain called the hippocampus*. Hippocampus is also the Latin name for seahorses (“hippo” is Greek for horse; “kampos”, amusingly, is Greek for sea-monster) and this brain area got its name because people thought it was shaped a bit like a seahorse. There’s a lot of this in science; it’s a more whimsical profession than you might think.

You may be wondering if this rather tenuous etymological connection is the only way in which this post is about fish. Certainly not! What this post is really about is episodic memory in fish. For a while after Tulving identified the different kinds of memory, people thought only humans were capable of episodic memory and that all the other animals only had semantic memories and were forever forgetting each other’s phone numbers. Discovering if this was true or not required finding a way to ask animals how detailed their memories of specific events were. Nicky Clayton and Tony Dickinson suggested that we should ask if the animal remembered, for one specific event, what happened, where it happened, and when (or how long ago) it happened. They then proceeded to demonstrate that scrub jays could remember all those aspects of a single food-storing event [2].

People later used this what-where-when criterion to look for episodic memory in other species. In some cases, the when part was replaced with changes in the context of the experiment, since animals generally don’t read clocks very well. For example, Madeline Eacott & Gillian Normann asked rats if they could remember what object they saw, where it was, and which room it was in [3]. I’ve drawn out their beautifully simple experiment below.
Picture
In the first part of the experiment (the left panel), they put the rats in the blue room with two objects (I’ve used a smiley face and a star; they used Coke cans and bits of plastic). Rats like to explore new things and so spent a lot of time exploring the objects. Then they were put in the second room (center panel), which was green, and contained the two objects in opposite locations. The rats had never seen the smiley face on the right before, nor the star on the left, and they’d never seen either item in a green room before, so the objects were still new-ish and they explored them. Finally, in the third stage (right panel), they were put back into the green room which now contained two stars. This is the important bit. The rats have seen the star before; they’ve seen a star in a green room before; they’ve seen a star on the left before and they’ve seen a star on the right before. They’re actually quite jaded rats. But there is a difference between the two stars: the rats have seen a star on the left in a green room, but they’ve never seen a star on the right in a green room. If you combine all three facts about the event: the room (context), the object (what), and the side (where), only one star is new (the one on the right). In the experiment, the rats explored that star more than the other one, demonstrating that they could remember all three things about their previous experiences. In other words, they showed that they have something that at least superficially resembles episodic memory (which researchers – who are cautious as well as whimsical – call “episodic-like”).
Ok, by now you might be getting pissed off about the lack of fish in this post. Well, here they are. Very recently, precisely the same experiment as described above has been done, successfully, with zebrafish [4]. The fish behaved almost exactly like the rats, showing that they could remember all three elements of a single experience, i.e., that they have episodic-like memory. This is especially cool because fish brains don’t have a hippocampus (which is ironic, since seahorses are fish; the hippocampus doesn’t have a hippocampus). Fish do have an area of the brain, called the medial pallium, which is thought to be similar to the mammalian hippocampus, but it has a completely different structure. So these fish are doing something we thought required a functioning hippocampus, but without having a hippocampus. In fact, Eacott and Norman showed that rats that had their hippocampus removed could no longer do the task.
So, not only do fish have quite good memories [see last post], but they also seem to have the same types of memory that we do. They can (probably) remember individual past events, like that weekend when you forgot to feed them, and what you were wearing then, and why it clashed with your handbag.


* This is a HUGE and painfully inaccurate over-simplification. However, this is a blog, not a textbook, and I can’t go into all the complexities of how different kinds of memory interact in different parts of the brain (even if we knew, which we mostly don’t). Let’s just say it’s really, really complicated.


  1. Tulving E (1972). Episodic and semantic memory. In Organization of Memory (Tulving & Donaldson, eds.), New York: Academic Press, pp. 381-403.
  2. Clayton NS, Dickinson A (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395:272-278.
  3. Eacott MJ, Norman G (2004). Integrated memory for object, place, and context in rats: a possible model of episodic-like memory? The Journal of Neuroscience, 24:1948-1953.
  4. Hamilton TJ, et al. (2016). Episodic-like memory in zebrafish. Animal Cognition, 19:1071-1079.
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Memento Dory

6/2/2017

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Goldfish
Fantails, from Mulertt's "Goldfish and their culture". Photo by Noam Miller.
Since this is my first post, I want to discuss fish memory, which is where I got the title for the blog: >3s (greater than 3 seconds). This comes from the myth that fish only have a 3-second memory, recently reinforced by the character of Dory in Disney’s Finding Nemo (and its sequel, Finding Dory). I haven’t been able to find the origin of the 3-second memory myth, but people that keep fish have known it to be false for a very long time. In 1883, Hugo Mulertt wrote The Goldfish and its Culture, which first popularized home aquaria (he also founded and owned the magazine The Aquarium, marketed his own line of fish food, and translated a book of German fish recipes to increase Americans’ consumption of fish). Mulertt had this to say:

        “Goldfish have a good memory; they will soon learn to know their master, remember their
        feeding-place and time. They can be trained to good manners, as they are easily influenced
        by their surroundings, and good qualities of individuals can be perpetuated in their
        offspring.” [1]


Ok, so he wasn’t so strong on how genetics works.

The kind of memory Mulertt mentions, learning when, where, and by whom they are fed, is the most common type of learning demonstrated in fish, and there are plenty of examples of it. Rainbow trout can remember that pressing a bar leads to food even after not seeing the bar for 3 months [2]; goldfish may remember a color that was paired with food for almost a year [3]; and one researcher who trained common rudd to eat out of his hand found that they would still eat of his hand (but not anybody else’s) after not seeing him for 6 months [4].

Some of the more impressive feats of fish memory involve spatial learning. Salmon, returning from a few years of adventure on the high seas, can identify the exact stream where they were spawned by its unique odor [5]. It smells like home. However, you can only smell which stream is home when you are already in the right river system. How do you get from the middle of the Pacific to the right river-mouth? Salmon, it seems, can use variations in the magnetic field of the earth to achieve this, which means they have to also remember what the strength of the field was at the mouth of the river when they left home, several years ago [6].

So why do people think that fish only have a 3-second memory? I can only speculate, but it might have something to do with the small round aquaria that goldfish are often kept in (like Elmo’s pet goldfish Dorothy, from Sesame Street, watched by millions of impressionable two-year olds). Maybe a child asked whether the fish get bored in so small a space and some well-meaning adult came up with the meme, little realizing how it would spread. I guess the moral of this is: when lying to children, keep in mind that they have memories every bit as good as the average goldfish.

  1. Mulertt, H. (1910). The goldfish and its culture. (Sixth ed.), p. 14.
  2. Adron JW, Grant PT, Cowey CB (1973). A system for the quantitative study of the learning capacity of rainbow trout and its application to the study of food preferences and behaviour. Journal of Fish Biology, 5:625-636.
  3. Pitcher T (2006). Foreword to Fish cognition and behavior, C Brown, K Laland, J Krause, eds. (Oxford: Blackwell), p. xvi.
  4. Bshary R, Wickler W, Fricke H (2002). Fish cognition: a primate’s eye view. Animal Cognition, 5:1-13.
  5. Hasler AD, Scholz AT (1983). Olfactory Imprinting and Homing in Salmon (Berlin: Springer).
  6. Putman NF, Lohman KJ, Putman EM, Quinn TP, Klimley AP, Noakes DLG (2013). Evidence for geomagnetic imprinting as a homing mechanism in Pacific salmon. Current Biology, 23:312-316.
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