Proximal CA1 20-40 Hz power dynamics reflect trial-specific information processing supporting nonspatial sequence memory
Abstract
The hippocampus is known to play a critical role in processing information about temporal context. However, it remains unclear how hippocampal oscillations are involved, and how their functional organization is influenced by connectivity gradients. We examined local field potential activity in CA1 as rats performed a nonspatial odor sequence memory task. We found that odor sequence processing epochs were characterized by distinct spectral profiles and proximo-distal CA1 gradients of theta and 20-40 Hz power than track running epochs. We also discovered that 20-40 Hz power was predictive of sequence memory performance, particularly in proximal CA1 and during the plateau of high power observed on trials in which animals had to maintain their decision until instructed to respond. Altogether, these results provide evidence that dynamics of 20-40 Hz power along the CA1 axis are linked to trial-specific processing of nonspatial information critical to order judgements and are consistent with a role for 20-40 Hz power in gating information processing.
Data availability
Data available on Dryad, Data DOI: doi:10.7280/D11960
-
Proximal CA1 20-40 Hz power dynamics reflect trial-specific information processing supporting nonspatial sequence memoryDryad Digital Repository, doi:10.7280/dryad.D11960.
Article and author information
Author details
Funding
National Science Foundation (CAREER Award IOS-1150292)
- Norbert J Fortin
National Science Foundation (BCS 1439267)
- Norbert J Fortin
National Institutes of Health (R01 MH115697)
- Norbert J Fortin
National Institutes of Health (R01 DC017687)
- Norbert J Fortin
National Institutes of Health (R01 MH102392)
- Michael A Yassa
National Institutes of Health (R01 AG053555)
- Michael A Yassa
National Institutes of Health (Training Grant T32 NS45540)
- Sandra Gattas
National Institutes of Health (Training Grant T32 DC010775)
- Gabriel A Elias
Whitehall Foundation (2010-05-84)
- Norbert J Fortin
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Laura L Colgin, University of Texas at Austin, United States
Ethics
Animal experimentation: All procedures were conducted in accordance with the guidelines from care and use of laboratory animals published by the National Institutes of Health. All animals were handled according to an approved Institutional Animal Care and Use Committee (IACUC) protocol (Protocol AUP-20-174).
Version history
- Received: January 28, 2020
- Preprint posted: March 10, 2020 (view preprint)
- Accepted: May 9, 2022
- Accepted Manuscript published: May 9, 2022 (version 1)
- Version of Record published: June 6, 2022 (version 2)
Copyright
© 2022, Gattas et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 711
- views
-
- 130
- downloads
-
- 3
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Genetics and Genomics
- Neuroscience
Genome-wide association studies have revealed >270 loci associated with schizophrenia risk, yet these genetic factors do not seem to be sufficient to fully explain the molecular determinants behind this psychiatric condition. Epigenetic marks such as post-translational histone modifications remain largely plastic during development and adulthood, allowing a dynamic impact of environmental factors, including antipsychotic medications, on access to genes and regulatory elements. However, few studies so far have profiled cell-specific genome-wide histone modifications in postmortem brain samples from schizophrenia subjects, or the effect of antipsychotic treatment on such epigenetic marks. Here, we conducted ChIP-seq analyses focusing on histone marks indicative of active enhancers (H3K27ac) and active promoters (H3K4me3), alongside RNA-seq, using frontal cortex samples from antipsychotic-free (AF) and antipsychotic-treated (AT) individuals with schizophrenia, as well as individually matched controls (n=58). Schizophrenia subjects exhibited thousands of neuronal and non-neuronal epigenetic differences at regions that included several susceptibility genetic loci, such as NRG1, DISC1, and DRD3. By analyzing the AF and AT cohorts separately, we identified schizophrenia-associated alterations in specific transcription factors, their regulatees, and epigenomic and transcriptomic features that were reversed by antipsychotic treatment; as well as those that represented a consequence of antipsychotic medication rather than a hallmark of schizophrenia in postmortem human brain samples. Notably, we also found that the effect of age on epigenomic landscapes was more pronounced in frontal cortex of AT-schizophrenics, as compared to AF-schizophrenics and controls. Together, these data provide important evidence of epigenetic alterations in the frontal cortex of individuals with schizophrenia, and remark for the first time on the impact of age and antipsychotic treatment on chromatin organization.
-
- Neuroscience
Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.