The hippocampal debate: are we asking the right questions?

Abstract

For years, the debate has been: 'Is the hippocampus the cognitive map?' or 'Is the hippocampus the core of memory?' These two hypotheses derived their original power from two key experiments-the cognitive map theory from the remarkable spatial correlates seen in recordings of hippocampal pyramidal cells and the memory theory from the profound amnesias seen in the patient H.M. Both of these key experiments have been reinterpreted over the years: hippocampal cells are correlated with much more than place and H.M. is missing much more than just his hippocampus. However, both theories are still debated today. The hippocampus clearly plays a role in both navigation and memory processing. The question that must be addressed is rather: 'What is the role played by the hippocampus in the navigation and memory systems?' By looking at the navigation system as a whole, one can identify the major role played by the hippocampus as correcting for accumulation errors that occur within idiothetic navigation systems. This is most clearly experimentally evident as reorientation when an animal is lost. Carrying this over to a more general process, this becomes a role of recalling a context, bridging a contextual gap, or, in other words, it becomes a form of recognition memory. I will review recent experimental data which seems to support this theory over the more general spatial or memory theories traditionally applied to hippocampus.

Grid cells: The position code, neural network models of activity, and the problem of learning

“…The general framework emerging from these investigations is consistent with numerous suggestions that preceded the discovery of grid cells (Sharp, 1999;Eichenbaum et al, 1999;Hartley et al, 2000;Redish, 2001;Gothard et al, 2001): that the idiothetic path integrator is likely to reside in the entorhinal cortex, while hippocampus takes as one of its inputs the idiothetically integrated position estimate, and combines it with input from various sensory modalities to perform further spatial (and nonspatial) associations and computations. Thus, grid cell input is neither necessary nor sufficient for spatial patterning in place cells in the presence of spatially informative sensory inputs (but it does play an important role in sharpening or improving the accuracy of spatial representations in the hippocampus (Brun et al, 2008b)), and it is necessary for driving place fields when external sensory cues are absent.…”

Path integration in mammals

“…debated (Redish, 2001), most investigators agree that spatial representation is at least one function of the hippocampus.…”

Neurocognitive aging: prior memories hinder new hippocampal encoding

“…For young rats, the hippocampal system is simulated as an attractor network, capable of maintaining a representation despite minor changes in external input from the EC. However, when the change in external context is sufficient, the circuit switches to a dramatically different representation [28,[90][91][92][93]. Upon entry into an environment, the balance of incoming sensory and stored information causes the hippocampal network to settle upon either the previously stored representation or a newly created representation.…”