Attention Enhances the Retrieval and Stability of Visuospatial and Olfactory Representations in the Dorsal Hippocampus

Abstract

Attention enhances the encoding and retrieval of olfactory and visuospatial representations by modulating place field stability, firing rate, and neuronal synchronization of pyramidal cells in the hippocampus.

Abstract

A key question in the analysis of hippocampal memory relates to how attention modulates the encoding and long-term retrieval of spatial and nonspatial representations in this region. To address this question, we recorded from single cells over a period of 5 days in the CA1 region of the dorsal hippocampus while mice acquired one of two goal-oriented tasks. These tasks required the animals to find a hidden food reward by attending to either the visuospatial environment or a particular odor presented in shifting spatial locations. Attention to the visuospatial environment increased the stability of visuospatial representations and phase locking to gamma oscillations—a form of neuronal synchronization thought to underlie the attentional mechanism necessary for processing task-relevant information. Attention to a spatially shifting olfactory cue compromised the stability of place fields and increased the stability of reward-associated odor representations, which were most consistently retrieved during periods of sniffing and digging when animals were restricted to the cup locations. Together, these results suggest that attention selectively modulates the encoding and retrieval of hippocampal representations by enhancing physiological responses to task-relevant information.

Author Summary

Attention modulates the encoding and retrieval of memories, but the physiological basis of this interaction has largely been unexplored. The formation of memories which depend on the hippocampus involves the conscious recall of events that occur in specific spatial contexts, a form of memory known as episodic. To investigate the physiological consequences of the interaction between attention and memory in the hippocampus, we recorded single-cell activity and local field potentials — the local rhythmic oscillatory activity of neurons — from the same cells over several days while animals learned one of two goal-oriented tasks. In the visuospatial version of the task, mice had to associate a specific spatial location with a reward, independent of an odor cue. In the nonspatial, olfactory version, mice had to associate a specific odor with the food reward, independent of spatial location. We found that, during periods of navigation, only neurons in the visuospatially trained animals displayed long-term stable representations of space, and neuronal synchronization to so-called gamma oscillations, a mechanism of signal amplification that has been proposed to underlie attentional processes. Conversely, when animals were sniffing the odors in fixed spatial locations, only neurons in the olfactory-trained group displayed a stable increase in firing rate in response to the reward-associated odor. Our data suggest that attention modulates what is encoded and retrieved by hippocampal cells and that neuronal synchronization to gamma oscillations may underlie the mechanism whereby attention leads to stable spatial memory retrieval during navigation.