The right hippocampus leads the bilateral integration of gamma-parsed lateralized information

  1. Nuria Benito
  2. Gonzalo Martín-Vázquez
  3. Julia Makarova
  4. Valeri A Makarov  Is a corresponding author
  5. Oscar Herreras  Is a corresponding author
  1. University Medical Center of the Johannes Gutenberg University, Germany
  2. Cajal Institute, Spain
  3. N.I. Lobachevsky State University of Nizhny Novgorod, Russia

Abstract

It is unclear whether the two hippocampal lobes convey similar or different activities and how they cooperate. Spatial discrimination of electric fields in anesthetized rats allowed us to compare the pathway-specific field potentials corresponding to the gamma-paced CA3 output (CA1 Schaffer potentials) and CA3 somatic inhibition within and between sides. Bilateral excitatory Schaffer gamma waves are generally larger and lead from the right hemisphere with only moderate covariation of amplitude, and drive CA1 pyramidal units more strongly than unilateral waves. CA3 waves lock to the ipsilateral Schaffer potentials, although bilateral coherence was weak. Notably, Schaffer activity may run laterally, as seen after the disruption of the connecting pathways. Thus, asymmetric operations promote the entrainment of CA3-autonomous gamma oscillators bilaterally, synchronizing lateralized gamma strings to converge optimally on CA1 targets. The findings support the view that interhippocampal connections integrate different aspects of information that flow through the left and right lobes.

Article and author information

Author details

  1. Nuria Benito

    Institute of Physiology, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Gonzalo Martín-Vázquez

    Department of Systems Neuroscience, Cajal Institute, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Julia Makarova

    Department of Systems Neuroscience, Cajal Institute, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Valeri A Makarov

    N.I. Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, Russia
    For correspondence
    vmakarov@mat.ucm.es
    Competing interests
    The authors declare that no competing interests exist.
  5. Oscar Herreras

    Department of Systems Neuroscience, Cajal Institute, Madrid, Spain
    For correspondence
    herreras@cajal.csic.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8210-3710

Funding

Ministerio de Economía y Competitividad (BFU2013-41533R)

  • Nuria Benito
  • Gonzalo Martín-Vázquez
  • Julia Makarova
  • Oscar Herreras

Russian Science Foundation (15-12-10018)

  • Valeri A Makarov

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The experiments were performed in accordance with European Union guidelines (2010/63/CE) and Spanish regulations (BOE 67/8509-12, 1988) regarding the use of laboratory animals. All of the animals were handled according to approved institutional Bioethics and Biosecurity Committee of the CSIC (ref:15/10/2014). The Ethics Committee for Animal Research at the Cajal Institute approved all the experimental protocols (Ref. CEEA-IC2011/011/CEI3/20131213). All surgery was performed under urethane anesthesia, and every effort was made to minimize suffering.

Copyright

© 2016, Benito 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

  • 2,448
    views
  • 411
    downloads
  • 38
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

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)

  1. Nuria Benito
  2. Gonzalo Martín-Vázquez
  3. Julia Makarova
  4. Valeri A Makarov
  5. Oscar Herreras
(2016)
The right hippocampus leads the bilateral integration of gamma-parsed lateralized information
eLife 5:e16658.
https://doi.org/10.7554/eLife.16658

Share this article

https://doi.org/10.7554/eLife.16658

Further reading

    1. Neuroscience
    Xiaoqian Yan, Sarah Shi Tung ... Kalanit Grill-Spector
    Research Article

    Organizing the continuous stream of visual input into categories like places or faces is important for everyday function and social interactions. However, it is unknown when neural representations of these and other visual categories emerge. Here, we used steady-state evoked potential electroencephalography to measure cortical responses in infants at 3–4 months, 4–6 months, 6–8 months, and 12–15 months, when they viewed controlled, gray-level images of faces, limbs, corridors, characters, and cars. We found that distinct responses to these categories emerge at different ages. Reliable brain responses to faces emerge first, at 4–6 months, followed by limbs and places around 6–8 months. Between 6 and 15 months response patterns become more distinct, such that a classifier can decode what an infant is looking at from their brain responses. These findings have important implications for assessing typical and atypical cortical development as they not only suggest that category representations are learned, but also that representations of categories that may have innate substrates emerge at different times during infancy.

    1. Neuroscience
    2. Stem Cells and Regenerative Medicine
    Desiree Böck, Maria Wilhelm ... Gerald Schwank
    Research Article

    Parkinson’s disease (PD) is a multifactorial disease caused by irreversible progressive loss of dopaminergic neurons (DANs). Recent studies have reported the successful conversion of astrocytes into DANs by repressing polypyrimidine tract binding protein 1 (PTBP1), which led to the rescue of motor symptoms in a chemically-induced mouse model of PD. However, follow-up studies have questioned the validity of this astrocyte-to-DAN conversion model. Here, we devised an adenine base editing strategy to downregulate PTBP1 in astrocytes and neurons in a chemically-induced PD mouse model. While PTBP1 downregulation in astrocytes had no effect, PTBP1 downregulation in neurons of the striatum resulted in the expression of the DAN marker tyrosine hydroxylase (TH) in non-dividing neurons, which was associated with an increase in striatal dopamine concentrations and a rescue of forelimb akinesia and spontaneous rotations. Phenotypic analysis using multiplexed iterative immunofluorescence imaging further revealed that most of these TH-positive cells co-expressed the dopaminergic marker DAT and the pan-neuronal marker NEUN, with the majority of these triple-positive cells being classified as mature GABAergic neurons. Additional research is needed to fully elucidate the molecular mechanisms underlying the expression of the observed markers and understand how the formation of these cells contributes to the rescue of spontaneous motor behaviors. Nevertheless, our findings support a model where downregulation of neuronal, but not astrocytic, PTBP1 can mitigate symptoms in PD mice.