Abstract
Processing of memory is supported by coordinated activity in a network of sensory, association, and motor brain regions. It remains a major challenge to determine where memory is encoded for later retrieval. Here we used direct intracranial brain recordings from epilepsy patients performing free recall tasks to determine the temporal pattern and anatomical distribution of verbal memory encoding across the entire human cortex. High gamma frequency activity (65-115 Hz) showed consistent power responses during encoding of subsequently recalled and forgotten words on a subset of electrodes localized in 16 distinct cortical areas activated in the tasks. More of the high gamma power during word encoding, and less power before and after the word presentation, was characteristic of successful recall and observed across multiple brain regions. Latencies of the induced power changes and this subsequent memory effect between the recalled and forgotten words followed an anatomical sequence from visual to prefrontal cortical areas. Finally, the magnitude of the memory effect was unexpectedly found to be the largest in selected brain regions both at the top and at the bottom of the processing stream. These included the language processing areas of the prefrontal cortex and the downstream visual areas at the junction of the occipital and temporal lobes. Our results provide evidence for distributed encoding of verbal memory organized along a hierarchical posterior-to-anterior processing stream.
Significance Statement Verbal memory is a complex function supported by a network of brain regions specialized for perception, decision-making, and execution of action. Our results shed light on the temporal and anatomical organization of this network during encoding of memories for subsequent recall. By finding consistent differences in fast gamma activity recorded directly from the human brain during presentation of words that were later recalled or forgotten, we identified specific regions with the greatest memory effect. This subsequent memory effect was present across a feed-forward processing stream, providing evidence for hierarchical and distributed organization of verbal memory. The identified brain regions in the processing stream present new targets for brain modulation technologies to treat verbal and cognitive deficits in brain disorders.
- cognition
- cortical mapping
- electrocorticography
- high frequency oscillations
- network oscillations
- short-term memory
Footnotes
Conflict of interest
M.J.K. and D.S.R. have started a company, Nia Therapeutics, LLC (‘Nia’), intended to develop and commercialize brain stimulation therapies for memory restoration. Each of them holds more than 5% equity interest in Nia.
Funding sources
This work was supported by the DARPA Restoring Active Memory (RAM) program (Cooperative Agreement N66001-14-2-4032). The views, opinions, and/or findings contained in this material are those of the authors and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government. Michal T. Kucewicz is supported from the First Team programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund. Vaclav Kremen was additionally supported by Czech Technical University in Prague.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
Jump to comment: