The Role of the Hippocampus in Solving the Morris Water Maze

Abstract

We suggest that the hippocampus plays two roles that allow rodents to solve the hidden-platform water maze: self-localization and route replay. When an animal explores an environment such as the water maze, the combination of place fields and correlational (Hebbian) long-term potentiation produces a weight matrix in the CA3 recurrent collaterals such that cells with overlapping place fields are more strongly interconnected than cells with nonoverlapping fields. When combined with global inhibition, this forms an attractor with coherent representations of position as stable states. When biased by local view information, this allows the animal to determine its position relative to the goal when it returns to the environment. We call this self-localization. When an animal traces specific routes within an environment, the weights in the CA3 recurrent collaterals become asymmetric. We show that this stores these routes in the recurrent collaterals. When primed with noise in the absence of sensory input, a coherent representation of position still forms in the CA3 population, but then that representation drifts, retracing a route. We show that these two mechanisms can coexist and form a basis for memory consolidation, explaining the anterograde and limited retrograde amnesia seen following hippocampal lesions.

The hippocampal debate: are we asking the right questions?

“…For example, the information represented in the hippocampal pyramidal cells during theta really seems to be the position of the animal within a context (see above). However, the information replayed during LIA states appears to be the recently traveled routes [139,178,206]. One possibility is that what is stored in the cortical memory is a habit-based route memory [178].…”

“…However, the information replayed during LIA states appears to be the recently traveled routes [139,178,206]. One possibility is that what is stored in the cortical memory is a habit-based route memory [178]. Intriguingly, this may be the normal transfer of memory from quickly-learned to slowlylearned mechanisms.…”

“…It can afford to be so because reinstantiation (recall) is computationally compatible with replay [173,178]. Theories of the computational function of hippocampus suggest that it has winner-take-all properties within an attractor network [111,173,196]: excitatory connections between pyramidal cells with overlapping place fields [241] and inhibitory feedback connections within the CA3 system force it to represent a single location [173,196].…”

“…The two roles can be implemented by a single attractor network with different boundary conditions [173,178]. If there are externally supplied inputs, then the network will find the coherent internal representation that is most consistent with those inputs [173,178,196,225].…”

“…If there are externally supplied inputs, then the network will find the coherent internal representation that is most consistent with those inputs [173,178,196,225]. But if there are no externally supplied inputs, then the network will still find a coherent representation of some random location.…”