Ripples synchronize activities in brain's cortex during sleep, waking

The research work was published in the Proceedings of the National Academy of Sciences (PNAS). Different elements of a memory, or mental event, are encoded in locations distributed across the brain's cortex. One hypothesis proposes that widespread networks are integrated with bursts of synchronized high-frequency oscillations, known as ripples, but evidence for the hypothesis is limited. Charles Dickey, Eric Halgren, and colleagues used intracranial recordings in 17 patients who were being monitored to localize seizure foci.

The results showed that 90-Hertz ripples, which lasted approximately 70 milliseconds, occurred simultaneously and had consistent phase lags across multiple distant cortical areas during sleep and waking. Memory recall is one cognitive process that requires linking different components of mental events into unified representations.

Before successful memory recall, the authors found, that ripple co-occurrence was enhanced between cortical sites and between the cortex and the hippocampus, which plays a crucial role in learning and memory. Together, the results suggest that brain ripples may support the binding of information into coherent experiences during memory retrieval.

Different elements of a memory, or any mental event, are encoded in locations distributed across the cortex. A prominent hypothesis proposes that widespread networks are integrated with bursts of synchronized high-frequency oscillations called "ripples," but the evidence is limited. Here, using recordings inside the human brain, we show that ripples occur simultaneously in multiple lobes in both cortical hemispheres and the hippocampus, generally during sleep and waking, and especially during memory recall.

Ripples phase-lock local cell firing and phase-synchronize with little decay between locations separated by up to 25 cm, enabling long-distance integration. Indeed, corippling sites have increased correlation of very-high-frequency activity which reflects cell firing. Thus, ripples may help bind information across the cortex in memory and other mental events.

Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such "binding" of different components of mental events into unified representations occurs is unknown. The "binding-by-synchrony" theory proposes that distributed encoding areas are bound by synchronous oscillations enabling enhanced communication. However, evidence for such oscillations is sparse.

Brief high-frequency oscillations ("ripples") occur in the hippocampus and cortex and help organize memory recall and consolidation. Here, using intracranial recordings in humans, we report that these 70-ms-duration, 90-Hz ripples often couple (within +-500 ms), co-occur (>= 25-ms overlap), and, crucially, phase-lock (have consistent phase lags) between widely distributed focal cortical locations during both sleep and waking, even between hemispheres. Cortical ripple co-occurrence is facilitated through activation across multiple sites, and phase-locking increases with more cortical site corippling. Ripples in all cortical areas co-occur with hippocampal ripples but do not phase-lock with them, further suggesting that cortico-cortical synchrony is mediated by cortico-cortical connections.

Ripple phase lags vary across sleep nights, consistent with participation in different networks. During waking, we show that hippocampo-cortical and cortico-cortical ripples increase preceding successful delayed memory recall when binding between the cue and response is essential. Ripples increase phase-modulated unit firing, and ripples increase high-frequency correlations between areas, suggesting synchronized unit spiking facilitates information exchange. co-occurrence, phase synchrony, and high-frequency correlation are maintained with little decrement over very long distances (25 cm). Hippocampal-cortico-cortical ripples appear to possess the essential properties necessary to support binding by synchrony during memory retrieval and perhaps generally in cognition. (ANI)