Viewpoints: how the hippocampus contributes to memory, navigation and cognition

Abstract

The hippocampus serves a critical function in memory, navigation, and cognition. Nature Neuroscience asked John Lisman to lead a group of researchers in a dialog on shared and distinct viewpoints on the hippocampus. There has been a long history of studying the hippocampus, but recent work has made it possible to study the cellular and network basis of defined operations—operations that include cognitive processes that have been otherwise difficult to study (see Box 1 for useful terminology). These operations deal with the context-dependent representation of complex memories, the role of mental exploration based on imagined rather than real movements, and the use of recalled information for navigation and decision-making. The progress that has been made in understanding the hippocampus has motivated the study of other brain regions that provide hippocampal input or receive hippocampal output; the hippocampus is thus serving as a nucleating point for the larger goal of understanding the neural codes that allow inter-regional communication and more generally, understanding how memory-guided behavior is achieved by large scale integration of brain regions. In generating a discussion among experts in the study of the cognitive processes of the hippocampus, the editors and I have posed questions that probe important principles of hippocampal function. We hope that the resulting discussion will make clear to readers the progress that has been made, while also identifying issues where consensus has not yet been achieved and that should be pursued in future research. – John Lisman

Time, memory, and the legacy of Howard Eichenbaum

“…This is an important discovery, and as I describe below, the findings also raise many fundamental questions about time, memory, and the hippocampus: 5.1 | What is the relationship between spatial and temporal coding? Although Eichenbaum coined the term "time cell," he was well aware that there are no such things as time or place cells (Lisman et al, 2017)-instead, he argued that hippocampal neurons encode "multiplexed maps of space and time" (Eichenbaum, 2017b). Studies of time cells indicate there is no obvious correspondence between the time and place fields of hippocampal neurons, suggesting that the hippocampus encodes space and time in parallel (Eichenbaum, 2014).…”

How the Hippocampus Represents Memories: Making Sense of Memory Allocation Studies

“…Hippocampal place cells are a case‐in‐point. Although place cells’ activity correlates with the position of the animal in a given environment and their activity is likely used to aid spatial navigation, a closer look at the evidence shows that those cells do not encode the animal's position per se . Place cells’ inputs deliver highly processed, multisensory information, which allows those cells to respond to a set of features that define a particular place in a particular environment .…”

“…Given the hippocampus’ functions, we would expect it to represent, somehow, information about the features of the episode being encoded. Indeed, the hippocampus seems to provide a framework to form relational representations of features of the episodes . It does so by integrating inputs from various brain regions, including multimodal sensory cortices (via entorhinal cortex), the amygdala, and the prefrontal cortex which, when combined, not only convey information about the different aspects of the episode but also allow the computations performed by the hippocampus to be modulated by emotional and attentional factors.…”

Differential reinforcement encoding along the hippocampal long axis helps resolve the explore/exploit dilemma

“…To learn such environments efficiently, we need to bind spatially and temporally coincident elements of experience into a cognitive map. Map representations found in the hippocampus help us link reinforcers to preceding actions, thereby revealing the best paths through the environment (Lisman et al, 2017). Hippocampal contributions to resolving the explore/exploit dilemma, however, have not been investigated using RL.…”