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The genomic underpinnings of oscillatory biomarkers supporting successful memory encoding in humans

ABSTRACT: Brain oscillations are remarkable components of brain activity that support memory encoding. However, it remains a major challenge to determine the molecular mechanisms underlining this activity in humans. Here, we used direct intracranial electroencephalography recordings from patients performing free recall tasks of verbal memory encoding in temporal cortex. Using resected tissue transcriptomics from the same patients, we linked gene expression with brain oscillations, identifying genes correlated with oscillatory signatures of memory formation across six frequency bands. Co-expression analysis isolated biomarker-specific modules associated with neuropsychiatric disorders as well as ion channel activity. Using single-nuclei transcriptomic data from resected tissue, we further revealed that biomarker-specific modules are enriched for both excitatory and inhibitory neurons. This unprecedented dataset of patient-specific brain oscillations coupled to genomics unlocks new insights into the genetic mechanisms that support memory encoding. By linking brain expression of these genes to oscillatory patterns, our data help overcome limitations of phenotypic methods to uncover genetic links to memory performance.

ORGANISM(S): Homo sapiens

PROVIDER: GSE139914 | GEO | 2020/12/09

REPOSITORIES: GEO

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Project description:Oscillatory phenomena are ubiquitous across different biological scales, from individual cells to tissues and whole organisms. In physical systems, oscillatory behaviour can emerge from weak coupling of independent stochastic elements. Once established, oscillations can drive coordinated group behaviour and encode robust information through oscillation frequency or amplitude. Here we use experimentation and modelling to understand the emergence and information coding properties of oscillatory cyclic adenosine monophosphate (cAMP) signaling in D. discoideum. Oscillatory cAMP signaling drives aggregation of individual amoebae and coordinated temporal shifts in gene expression. However, it is unknown how the collective behaviour emerges and attenuates in an auto-regulatory manner where temporal transcriptional regulation must decode variation in cAMP pulse count, frequency, or amplitude. To address these questions, we identified a transcription factor, Hbx5, that is essential for the initiation of collective behaviour and its activity provides a single-cell readout of the earliest sign of cAMP signaling. This reveals stochastic pulses in cAMP signaling precede collective oscillations, with Hbx5 dependent transcriptional feedback enhancing signal sensitivity necessary for the emergence of collective oscillations. We demonstrate that once collective oscillations have been established, another cAMP-regulated transcription factor, GtaC, required for subsequent developmental progression becomes activated. Modelling and experimentation suggest that temporal differences in transcription factor activation arise from differences in the threshold at which the protein kinase, ErkB, influences their activity. This leads us to propose that changes in the amplitude of cAMP oscillations during development encode temporal information, driving the orderly progression of development. These studies thus provide crucial insights into the principles driving collective behaviour and the evolution of multicellular systems.

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The genomic underpinnings of oscillatory biomarkers supporting successful memory encoding in humans

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