Mechanisms for widespread hippocampal involvement in cognition

Abstract

The quintessential memory system in the human brain--the hippocampus and surrounding medial temporal lobe--is often treated as a module for the formation of conscious, or declarative, memories. However, growing evidence suggests that the hippocampus plays a broader role in memory and cognition and that theories organizing memory into strictly dedicated systems may need to be updated. We first consider the historical evidence for the specialized role of the hippocampus in declarative memory. Then, we describe the serendipitous encounter that motivated the special section in this issue, based on parallel research from our labs that suggested a more pervasive contribution of the hippocampus to cognition beyond declarative memory. Finally, we develop a theoretical framework that describes 2 general mechanisms for how the hippocampus interacts with other brain systems and cognitive processes: the memory modulation hypothesis, in which mnemonic representations in the hippocampus modulate the operation of other systems, and the adaptive function hypothesis, in which specialized computations in the hippocampus are recruited as a component of both mnemonic and nonmnemonic functions. This framework is consistent with an emerging view that the most fertile ground for discovery in cognitive psychology and neuroscience lies at the interface between parts of the mind and brain that have traditionally been studied in isolation.

Figure 1

(A) Incidental exposure to temporal regularities increases the similarity of voxel patterns elicited by the associated objects within the hippocampus (Schapiro et al., 2012). This representational similarity allows the perception of one object to partially reactivate the hippocampal representation of the associate. (B) The extent to which this occurs during reward learning for one of the objects, as reflected in overall hippocampal activation, determines the value of the other associated object (Wimmer & Shohamy, 2012). This value is reflected in a higher likelihood of choosing this object later during decision-making, even when it itself has never been directly rewarded. This figure is a conceptual depiction of the overlap of the studies in our two labs; in Wimmer & Shohamy (2012), S1 images were actually faces, body parts, or scenes, rather than fractals.

Figure 2

(A) Meta-analysis from http://neurosynth.org (see Yarkoni, Poldrack, Nichols, Van Essen, & Wager, 2011) of more than 4000 published studies illustrating multiple brain regions associated with episodic memory. Colored voxels reflect a significant probability of the term “episodic” appearing in articles that reported activation in these voxels (reverse inference, corrected p < 0.05). (B) Meta-analysis of the same database illustrating multiple functions associated with the hippocampus and MTL (white frame). Colored voxels reflect a significant probability of activation in these voxels when an article contained each of the terms (forward inference, corrected p < 0.05).

Figure 3

(A) The hippocampus is highly interconnected with many other cortical and subcortical brain regions, including those traditionally thought to support separate memory systems. These anatomical connections provide opportunities for shared and interactive cognitive processing. (B) Information processing circuit among subfields of the hippocampus. Amyg = amygdala; CA# = cornu ammonis area #; DG = dentate gyrus; EC = entorhinal cortex; GP = globus pallidus; NAcc = nucleus accumbens; PHC = parahippocampal cortex; PRC = perirhinal cortex; Sub = subiculum; VTA = ventral tegmental area.

Figure 4

(A) The Memory Modulation Hypothesis posits that mnemonic representations are the currency of the hippocampus, and that these representations bias other cognitive processes. This can occur transiently, by reactivating related experiences from the past and making them available to active processes, or more permanently, via offline consolidation of cortical and subcortical connections. (B) The Adaptive Function Hypothesis posits that the hippocampus has special computational properties, such as recurrence, sparse coding, rapid binding, and massive interconnectedness, which make it useful for various mnemonic and non-mnemonic cognitive processes. Other than these unique properties, however, it is like any other system — it receives input from upstream, performs certain computations, and sends output downstream. In both panels, the circles reflect neurons or neuronal ensembles, the lines reflect undirected synaptic connections, the processes subserve different cognitive functions, and the stages reflect different brain regions or the same brain region at different timesteps.