# Attractors in memory: A perspective

Bruno Poucet, Etienne Save

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Bruno Poucet, Etienne Save. Attractors in memory: A perspective. Science, 2005, 308 (5723), pp.799-800. 10.1126/science.1112555. hal-00093873

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# Attractors in Memory

Bruno Poucet and Etienne Save

One of the most challenging questions facing contemporary neuroscience is how the brain encodes the memories of an individual's experiences. Within this broad question, the issue of how the brain makes a distinction between separate yet similar episodes is crucial. By recording the electrical discharges of neurons in the brains of animals performing different behavioral tasks, it is possible to decipher some of the rules governing this process. On page 873 of this issue, Wills et al. (1) suggest that memories are like attractor states in which all neurons abruptly and simultaneously change their electrical discharges in relation to the current experiences of the rats under study. To demonstrate this, Wills et al. recorded the firing activity of hippocampal place cells in the brains of freely moving rats exposed to a square or circular environment (see the figure).

The authors observed the neural activity of hippocampal place cells by recording spike activity from single hippocampal pyramidal neurons and simultaneously tracking the location of the rat in the environment. Each place cell discharges only when the animal is in a cell-specific stable region called its “place field.” Place fields occur with about equal density over the entire surface of the environment, hence their ensemble firing can be decoded to determine the animal’s location in space (2). Although place fields are stable across days and weeks in constant surroundings (3), they undergo great variation if large changes are made in the environment. Thus, changing the shape of the environment for example, from a circle to a square causes major modifications in the activity of all place cells (see the figure). Some place cells have fields in only one of the two environments and are silent in the other, whereas the fields of cells active in both environments are quite different in shape or location. Such changes, known as remappings, occur most reliably after modifying the shape of the environment, but also appear after more subtle changes (4, 5). The remapping phenomenon suggests that the hippocampus learns and

holds distinct maps for distinct contexts, with each specific map being reactivated as the rat commutes between the different contexts (6). Thus, place cells signal both the rat's current environment and its location within that environment.

<figure><img src="image_2.png" /><figcaption>B</figcaption></figure>

<figure><img src="image_3.png" /><figcaption>C</figcaption></figure>

<figure><img src="image_4.png" /><figcaption>D</figcaption></figure>

<figure><img src="image_5.png" /></figure>

**Changing shapes.** Rats exposed to a square or circular environment evoke distinct representations in "place" neurons of the hippocampus (7). (A) The place fields (white ellipses) are different for the circular and square environments. (B) When the rat is exposed to an intermediate shape (such as an octagon), all place cells simultaneously adopt one of the two learned activity patterns (the square in the example). (C) This observation reveals that the activity states of place cells are under the control of attractor like mechanisms. (D) With experience, new attractors may develop so that intermediate shapes are represented.

Given that remapping reflects the learning process of a new environment, it is of interest to investigate its time course. Remapping may be very rapid, taking place in a matter of minutes when the rat moves freely from a familiar environment to a new one (2). In contrast, a slower variable rat-specific time course is observed when the rat is brought from a familiar environment (such as a square) to a new environment (such as a circle) (7). At first, the place fields are equivalent in both environments. With additional exposures to the circle, however, the fields of a progressively greater fraction of cells become distinct. Not only does this map differentiation occur at different rates in different rats, it also occurs at different rates for cells within a given rat. Gradual shifts in the place fields may be seen for individual place cells. Ultimately, however, discrimination of the square and circle appears to go to completion so that the fields of all cells become distinct.

What is the neural correlate of this discrimination once it is established? Wills et al. tackled this issue by using a series of “morph” boxes. Each morph box was made of a number of juxtaposed plastic elements that could be arranged in a variety of configurations. The overall geometry of the box could be varied from a circle to a square through four intermediate octagonal shapes, from more circular-like to more square-like. Rats were first extensively exposed to a wooden circle and to a square made of morph material. This ensured the rapid occurrence of remapping, which persisted when rats were exposed to circular and square boxes both made of morph material. Then Wills et al. exposed rats to a series of morph boxes in a pseudo-random order across successive recording sessions.

What became of the place fields when rats were exposed to morph boxes of intermediate shape? Wills et al. found that most cells adopted either the circle-like or square-like pattern in the morph boxes and almost never exhibited other patterns. The switch from one activity pattern to the other was abrupt, and the switch point was for the morph box whose shape was approximately at the midpoint between a circle and a square (see the figure). Not only was the switch point similar for all rats, it was also the same for all simultaneously recorded cells within a given rat. Because only the geometry of the recording box varied across successive exposures, such effects were unambiguously caused by changes in environmental shape. Interestingly, the same abrupt changes in place fields were seen on

<footnote>The authors are in the Laboratory of Neurobiology and Cognition, CNRS Université Aix Marseille, Centre Saint Charles, 13331 Marseille Cedex 3, France. E mail: bpoucet@up.univ mrs.fr</footnote>
a second series of exposures to the morph
boxes, although in some rats the shift point
could vary from that displayed during the
initial presentation. Moreover, the firing pat-
terns within a session were established very
rapidly, usually within the first 30 seconds.

What do these results suggest about the
neural processes of memory in the brain?
First, all place cells were seen to switch
abruptly between two distinct states across
successive sessions, which seems to indi-
cate the operation of attractors. Such attrac-
tors induce the hippocampal system to
adopt one of the two possible activity states
triggered by the two well-learned box
shapes. This major property of hippocampal
representation is akin to pattern separation,

which allows slightly different inputs to
result in distinct output representations.
Such a process reduces interference
between similar experiences and comple-
ments another process necessary for mem-
ory retrieval; pattern completion, in which
an autoassociative network recalls stored
patterns based on incomplete information
(8). Second, the results reveal that the hip-
pocampal place cell system can build cate-
gories within which the representation of
each intermediate box shape is nested.
Although these properties of pattern separa-
tion and categorization are useful for initial
encoding of new experiences within famil-
iar contexts, they must also be accompanied
by additional mechanisms that allow incre-

mental storage of new contexts. Thus, with
repeated exposure, the geometry of a new
environment could ultimately lead to a new
activity state that may permit the encoding
of new memories (7).

References

1. T. J. Wills, C. Lever, F. Cacucci, N. Burgess, J. O'Keefe, *Science* **308**, 873 (2005).

2. M. A. Wilson, B. L. McNaughton, *Science* **261**, 1055 (1993).

3. L. T. Thompson, P. J. Best, *Brain Res.* **509**, 299 (1990).

4. R. U. Muller, J. L. Kubie, *J. Neurosci.* **7**, 1951 (1987).

5. C. Kentros et al., *Science* **280**, 2121 (1998).

6. V. Paz-Villagrán et al., *Eur. J. Neurosci.* **20**, 1379 (2004).

7. C. Lever et al., *Nature* **416**, 90 (2002).

8. J. F. Guzowski et al., *Neuron* **44**, 581 (2004).