Different theories of the hippocampus hold that it represents spatial information or episodic memories. Much of our research has focused on a different, but closely related idea: that the hippocampus represents contextual information, which includes spatial information and is a critical substrate for episodic memories. We study the neural processing of contextual information and the ways in which contextual cues promote the retrieval of behavioral responses and memories. It is well-known that hippocampal neurons exhibit distinct firing patterns in different environments (i.e. remapping). Indeed, the patterns of neuronal activity are so distinct that they could serve as a neural representation of the context. These context representations could, through learning processes, become associated with the memories and behavioral responses appropriate to that context. This provides a mechanistic explanation for the well-documented phenomenon in which the context primes memories and behavioral responses.
Interestingly, contexts need not be defined solely by the spatial environment, but can also be defined by the task demands, expectations and other behavioral variables. For example, hippocampal neurons ‘remap’ in response to changes in task rules even when the environment die not change (Fig. 1). More recently, we found that the hippocampus treats different task epochs (trials and inter-trial periods) as coherent contexts (Bulkin et al., 2019). We also found that the quality of hippocampal firing patterns (i.e. how distinct they are at any given moment) predicts how well subjects will be able to retrieve the memories that belong to that context. This provides a key link between hippocampal firing patterns and contextual memory (Bulkin et al., 2016).
Figure 1.
Hippocampal neurons exhibited remarkably different place fields and reward responses when rats performed a plus maze task in two different contexts. The top plots show an example of a hippocampal neuron that had a place field in one context (red contour) but not the other. The bottom plots show an example of a neuron that fired when the rat obtained a reward in one context but not in the other context.
Bulkin, D.A., Sinclair, D.G., Law, L.M., & Smith, D. M. (2019). Hippocampal state transitions at the boundaries between trial epochs. Hippocampus. https://doi.org/10.1002/hipo.23180 
Bulkin, D. A., Law, L. M., & Smith, D. M. (2016). Placing memories in context: Hippocampal representations promote retrieval of appropriate memories. Hippocampus, 26(7), 958–971. https://doi.org/10.1002/hipo.22579
Smith, D. M., & Bulkin, D. A. (2014). The form and function of hippocampal context representations. Neuroscience & Biobehavioral Reviews, 40, 52–61. https://doi.org/10.1016/j.neubiorev.2014.01.005
Butterly, D. A., Petroccione, M. A., & Smith, D. M. (2012). Hippocampal context processing is critical for interference free recall of odor memories in rats. Hippocampus, 22(4), 906–913. https://doi.org/10.1002/hipo.20953
Smith, D. M., Barredo, J., & Mizumori, S. J. Y. (2012). Complimentary roles of the hippocampus and retrosplenial cortex in behavioral context discrimination. Hippocampus, 22(5), 1121–1133. https://doi.org/10.1002/hipo.20958
