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Learning-Enhanced Coupling between Association Cortices and Hippocampus
Science 20 Oct 2017: Vol. 358, Issue 6361, pp. 369-372 Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus Dion Khodagholy, et.al. NYU Neuroscience Institute, School of Medicine, New York University, New York, NY 10016, USA. Department of Electrical Engineering, Columbia University, New York, NY 10027, USA. Department of Neurology, Columbia University Medical Center, New York, NY 10032, USA. Institute for Genomic Medicine, Columbia University Medical Center, New York, NY 10032, USA. [paraphrase] Consolidation of declarative memories requires hippocampal-neocortical communication. Although experimental evidence supports the role of sharp-wave ripples in transferring hippocampal information to the neocortex, the exact cortical destinations and the physiological mechanisms of such transfer are not known. We used a conducting polymer-based conformable microelectrode array (NeuroGrid) to record local field potentials and neural spiking across the dorsal cortical surface of the rat brain, combined with silicon probe recordings in the hippocampus, to identify candidate physiological patterns. Parietal, midline, and prefrontal, but not primary cortical areas, displayed localized ripple (100 to 150 hertz) oscillations during sleep, concurrent with hippocampal ripples. Coupling between hippocampal and neocortical ripples was strengthened during sleep following learning. These findings suggest that ripple-ripple coupling supports hippocampal-association cortical transfer of memory traces. Association neocortex is an evolutionarily recent type of cortex characterized by higher-order neural circuits that mediate multimodal, advanced information processing related to cognition. A key unifying feature of association cortices is their strong reciprocal anatomical and functional connectivity with medial temporal lobe structures. This connectivity is required for consolidation of declarative memory, which involves the transfer of information rapidly encoded in the hippocampus to long-term storage. Consolidation of hippocampus-dependent memory is accompanied by increased immediate early gene expression and structural changes in neural networks of association cortices. High-frequency, synchronous hippocampal oscillations, called ripples, are implicated in mediating memory consolidation by distributing compressed representations of waking experience to interconnected cortical networks during periods of quiescence or slow-wave sleep. Hippocampal ripples have been temporally linked to cortical sleep spindles and patterned neuronal firing in certain association cortices. Occurrence of hippocampal ripples is likewise influenced by ongoing cortical oscillations and is linked to whole-brain patterns of activation and deactivation over an extended time scale relative to ripple duration. In this study, we have identified ripple frequency oscillations that were present in association but not in primary sensory cortical areas. These association areas, including parietal, retrosplenial, anterior cingulate, and medial prefrontal cortex, are reciprocally anatomically and functionally connected with medial temporal lobe structures and exhibit extensive corticocortical connections. Hippocampal and neocortical ripples co-occur in these areas, reflecting either a direct hippocampal–entorhinal cortex–neocortex excitation or an indirect common drive by cortical slow oscillations. The coordination of cortical ripples with “down” to “up” state transitions, and the correlation of both hippocampal and cortical ripples with sleep spindles, suggests that cortical ripples may form part of the hippocampal-cortical dialogue during NREM sleep. Following induction of long-term hippocampal-dependent memory, coupling of hippocampal and neocortical ripples increased significantly. Analogous to hippocampal ripples, cortical ripples may signify information transfer involving association cortex. Overall, our findings suggest that ripple oscillation mechanisms of NREM sleep in both hippocampal and neocortical association areas support memory consolidation. [end of paraphrase]
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