Is hippocampal remapping the physiological basis for context?

Abstract

In 1980, Nadel and Wilner extended Richard Hirsh's notion that the hippocampus creates environmental representations, called “contexts,” suggesting that the fundamental structure of context was the spatial representation proposed by O'Keefe and Nadel's landmark book, The Hippocampus as a Cognitive Map (1978). This book, in turn, derives from the discovery that individual hippocampal neurons act as place cells, with the complete set of place cells tiling an enclosure, forming a type of spatial map. It was found that unique environments had unique place cell representations. That is, if one takes the hippocampal map of a specific environment, this representation scrambles, or “remaps” when the animal is placed in a different environment. Several authors have speculated that “maps” and “remapping” form the physiological substrates for context and context shifting. One difficulty with this definition is that it is exclusively spatial; it can only be inferred when an animal locomotes in an enclosure. There are five aims for this article. The first is to give an historical overview of context as a variable that controls behavior. The second aim is to give an historical overview of concepts of place cell maps and remapping. The third aim is to propose an updated definition of a place cell map, based on temporal rather than spatial overlaps, which adds flexibility. The fourth aim is to address the issue of whether the biological phenomenon of hippocampal remapping, is, in fact, the substrate for shifts in the psychological phenomenon of context. The final aim is speculation of how contextual representations may contribute to effective behavior.

An emergent neural coactivity code for dynamic memory

“…In this study we observe that contingency discriminating coactivity is not a reflection of spatial remapping. Instead, our findings are consistent with the view that spatial remapping may be a specific instance of a more general phenomenon of “temporal remapping”, in which the short-timescale temporal correlation structure of neurons differs across distinct contexts 23 . Indeed, in tasks where animals must disambiguate different spatial reference frames, millisecond timescale coactivity is a robust correlate of moment-by-moment behavioural discrimination of different contexts, both in networks that show spatial remapping 22 and those that do not 25 .…”

“…Our findings also provide new insights into the role of correlated neural activity in guiding contextual behaviour. Spatial remapping, where patterns of spatial correlations between hippocampal principal cells disambiguate distinct spatial contexts, has been proposed as a neural basis for contextual learning 23 . In this study we observe that contingency discriminating coactivity is not a reflection of spatial remapping.…”

“…Given the potential for rapid stabilization and retrieval of neural codes based on millisecond-timescale coactivity, such codes may support behavioural performance when animals must rapidly learn and flexibly retrieve salient information – a process we refer to here as “ dynamic memory ”. Converging evidence suggests a prominent role of the hippocampus for such rapid and flexible learning 21 – 23 , supporting models that frame the hippocampus as a fast learning system 24 . Moreover, neural activity in the hippocampus is organized into temporally precise coactivity patterns 15 , 22 , 25 .…”

Memory Traces Diminished by Exercise Affect New Learning as Proactive Facilitation

“…During reversal learning with high interference, the rewarded pairs were reversed (i.e., rewarded for responding to odor 2 in context A and to odor 1 in context B). Based on the hippocampal cognitive map theory, each context corresponds to a specific hippocampal map (environmental cues influence behavior), and "remapping" occurs when the context changes (Kubie et al, 2019). Therefore, there are two maps in the paired-associate task and two "remapping" processes during reversal learning.…”

“…During reversal learning for the WMT groups, we found a lingering exploration of the former TQ in the sedentary group, which might explain the lower learning efficiency in the sedentary group when compared with the exercise group. During reversal learning, hippocampal remapping occurs, and another set of place cells is activated (Kubie et al, 2019). Adult-born neurons are more sensitive than mature neurons in responding to stimulation (Beining et al, 2017).…”