The what and when of olfactory working memory in humans

Authors

Andrew I. Yang, Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: iyang.and@gmail.com.Follow
Gulce N. Dikecligil, Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA.
Heidi Jiang, Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
Sandhitsu R. Das, Department of Radiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Joel M. Stein, Department of Radiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Stephan U. Schuele, Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
Joshua M. Rosenow, Department of Neurosurgery, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
Kathryn A. Davis, Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Timothy H. Lucas, Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Jay A. Gottfried, Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: jaygottf@pennmedicine.upenn.edu.

Document Type

Article

Abstract

Encoding and retaining novel sequences of sensory stimuli in working memory is crucial for adaptive behavior. A fundamental challenge for the central nervous system is to maintain each sequence item in an active and discriminable state, while also preserving their temporal context. Nested neural oscillations have been postulated to disambiguate the "what" and "when" of sequences, but the mechanisms by which these multiple streams of information are coordinated in the human brain remain unclear. Drawing from foundational animal studies, we recorded local field potentials from the human piriform cortex and hippocampus during a working memory task in which subjects experienced sequences of three distinct odors. Our data revealed a unique organization of odor memories across multiple timescales of the theta rhythm. During encoding, odors elicited greater gamma at distinct theta phases in both regions, time stamping their positions in the sequence, whereby the robustness of this effect was predictive of temporal order memory. During maintenance, stimulus-driven patterns of theta-coupled gamma were spontaneously reinstated in piriform cortex, recapitulating the order of the initial sequence. Replay events were time compressed across contiguous theta cycles, coinciding with periods of enhanced piriform-hippocampal theta-phase synchrony, and their prevalence forecasted subsequent recall accuracy on a trial-by-trial basis. Our data provide a novel link between endogenous replay orchestrated by the theta rhythm and short-term retention of sequential memories in the human brain.

Medical Subject Headings

Animals; Hippocampus (physiology); Humans; Memory, Short-Term (physiology); Piriform Cortex (physiology); Smell; Theta Rhythm (physiology)

Publication Date

10-25-2021

Publication Title

Current biology : CB

E-ISSN

1879-0445

Volume

31

Issue

20

First Page

4499

Last Page

4511.e8

PubMed ID

34450088

Digital Object Identifier (DOI)

10.1016/j.cub.2021.08.004

Recommended Citation

Yang, Andrew I.; Dikecligil, Gulce N.; Jiang, Heidi; Das, Sandhitsu R.; Stein, Joel M.; Schuele, Stephan U.; Rosenow, Joshua M.; Davis, Kathryn A.; Lucas, Timothy H.; and Gottfried, Jay A., "The what and when of olfactory working memory in humans" (2021). Neurosurgery. 1888.
https://scholar.barrowneuro.org/neurosurgery/1888