A Signature of Attractor Dynamics in the CA3 Region of the Hippocampus

Abstract

The notion of attractor networks is the leading hypothesis for how associative memories are stored and recalled. A defining anatomical feature of such networks is excitatory recurrent connections. These “attract” the firing pattern of the network to a stored pattern, even when the external input is incomplete (pattern completion). The CA3 region of the hippocampus has been postulated to be such an attractor network; however, the experimental evidence has been ambiguous, leading to the suggestion that CA3 is not an attractor network. In order to resolve this controversy and to better understand how CA3 functions, we simulated CA3 and its input structures. In our simulation, we could reproduce critical experimental results and establish the criteria for identifying attractor properties. Notably, under conditions in which there is continuous input, the output should be “attracted” to a stored pattern. However, contrary to previous expectations, as a pattern is gradually “morphed” from one stored pattern to another, a sharp transition between output patterns is not expected. The observed firing patterns of CA3 meet these criteria and can be quantitatively accounted for by our model. Notably, as morphing proceeds, the activity pattern in the dentate gyrus changes; in contrast, the activity pattern in the downstream CA3 network is attracted to a stored pattern and thus undergoes little change. We furthermore show that other aspects of the observed firing patterns can be explained by learning that occurs during behavioral testing. The CA3 thus displays both the learning and recall signatures of an attractor network. These observations, taken together with existing anatomical and behavioral evidence, make the strong case that CA3 constructs associative memories based on attractor dynamics.

Author Summary

A type of neural network called an “attractor network” is thought to underlie memory associations. Importantly, when such a network is presented with part of a memory, the network activity is attracted to the complete memory. However, it has been difficult to obtain clear experimental evidence for such attractor networks. Indeed, recent “morphing” experiments that were specifically designed to observe these attractor dynamics in the hippocampus did not obtain the expected results, leading to a controversy on the validity of the attractor hypothesis of memory. Here, we have built a computational model of the relevant hippocampal areas, including its core anatomical and physiological features, and through the use of large-scale computer simulations reveal in detail the physiological properties expected of the hippocampal attractor network during morphing experiments. We show that the experimental results obtained are actually those to be expected of an attractor network when the specifics of the experimental protocol are taken into account. Most importantly, the results directly demonstrate the attraction of CA3 activity to a stored pattern. Our results, together with previous behavioral and in vitro studies, provide strong evidence that CA3 is an attractor network for associative memory.