Persistent activity during working memory maintenance predicts long-term memory formation in the human hippocampus

Jonathan Daume; Jan Kamiński; Yousef Salimpour; Andrea Gómez Palacio Schjetnan; William S Anderson; Taufik A Valiante; Adam N Mamelak; Ueli Rutishauser

doi:10.1016/j.neuron.2024.09.013

Persistent activity during working memory maintenance predicts long-term memory formation in the human hippocampus

Neuron. 2024 Oct 10:S0896-6273(24)00661-5. doi: 10.1016/j.neuron.2024.09.013. Online ahead of print.

Authors

Jonathan Daume¹, Jan Kamiński², Yousef Salimpour³, Andrea Gómez Palacio Schjetnan⁴, William S Anderson³, Taufik A Valiante⁵, Adam N Mamelak⁶, Ueli Rutishauser⁷

Affiliations

¹ Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Center for Neural Science and Medicine, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA.
² Center of Excellence for Neural Plasticity and Brain Disorders: BRAINCITY, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland.
³ Department of Neurosurgery, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA.
⁴ Krembil Research Institute, University Health Network, Toronto, ON M5T 2S8, Canada.
⁵ Krembil Research Institute, University Health Network, Toronto, ON M5T 2S8, Canada; Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, ON M5T 1P5, Canada; Department of Electrical and Computer Engineering, Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, ON M5S 3G9, Canada.
⁶ Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA.
⁷ Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Center for Neural Science and Medicine, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA. Electronic address: ueli.rutishauser@cshs.org.

PMID: 39406238
DOI: 10.1016/j.neuron.2024.09.013

Abstract

Working memory (WM) and long-term memory (LTM) are often viewed as separate cognitive systems. Little is known about how these systems interact when forming memories. We recorded single neurons in the human medial temporal lobe while patients maintained novel items in WM and completed a subsequent recognition memory test for the same items. In the hippocampus, but not in the amygdala, the level of WM content-selective persistent activity during WM maintenance was predictive of whether the item was later recognized with high confidence or forgotten. By contrast, visually evoked activity in the same cells was not predictive of LTM formation. During LTM retrieval, memory-selective neurons responded more strongly to familiar stimuli for which persistent activity was high while they were maintained in WM. Our study suggests that hippocampal persistent activity of the same cells supports both WM maintenance and LTM encoding, thereby revealing a common single-neuron component of these two memory systems.

Keywords: amygdala; category-selective neurons; confidence ratings; declarative memory; hippocampus; human single-neuron recordings; long-term memory; memory-selective neurons; persistent activity; working memory.

Grants and funding

U01 NS117839/NS/NINDS NIH HHS/United States