RT Journal Article
SR Electronic
T1 Human verbal memory encoding is hierarchically distributed in a continuous processing stream
JF eneuro
JO eNeuro
FD Society for Neuroscience
SP ENEURO.0214-18.2018
DO 10.1523/ENEURO.0214-18.2018
A1 Michal T Kucewicz
A1 Krishnakant Saboo
A1 Brent M Berry
A1 Vaclav Kremen
A1 Laura R Miller
A1 Fatemeh Khadjevand
A1 Cory S Inman
A1 Paul Wanda
A1 Michael R Sperling
A1 Richard Gorniak
A1 Kathryn A Davis
A1 Barbara C Jobst
A1 Bradley Lega
A1 Sameer A Sheth
A1 Daniel S Rizzuto
A1 Ravishankar K Iyer
A1 Michael J Kahana
A1 Gregory A Worrell
YR 2019
UL http://www.eneuro.org/content/early/2019/01/22/ENEURO.0214-18.2018.abstract
AB 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.