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      Ventral hippocampal OLM cells control type 2 theta oscillations and response to predator odor

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          Abstract

          Dorsal and ventral hippocampus regions exert cognition and emotion-related functions, respectively. Since both regions display rhythmic activity, specific neural oscillatory pacemakers may underlie their functional dichotomy. Type 1 theta oscillations are independent of cholinergic transmission and are observed in the dorsal hippocampus during movement and exploration. In contrast, type 2 theta depends on acetylcholine and appears when animals are exposed to emotionally laden contexts such as a predator presence. Despite its involvement in emotions, type 2 theta has not been associated with the ventral hippocampus. Here, we show that optogenetic activation of oriens-lacunosum moleculare (OLM) interneurons in the ventral hippocampus drives type 2 theta. Moreover, we found that type 2 theta generation is associated with increased risk-taking behavior in response to predator odor. These results demonstrate that two theta oscillations subtypes originate in the two hippocampal regions that predominantly underlie either cognitive or emotion-related functions.

          Abstract

          There are two subtypes of hippocampal theta oscillations that differ in frequency range, pharmacology, and behavioural correlates. Here, the authors report that activity of OLM interneurons in the ventral hippocampus mediates type 2 theta, associated with increased risk-taking in the presence of predator threat.

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          Most cited references51

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          Theta oscillations in the hippocampus.

          Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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            Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering.

            This study introduces a new method for detecting and sorting spikes from multiunit recordings. The method combines the wavelet transform, which localizes distinctive spike features, with superparamagnetic clustering, which allows automatic classification of the data without assumptions such as low variance or gaussian distributions. Moreover, an improved method for setting amplitude thresholds for spike detection is proposed. We describe several criteria for implementation that render the algorithm unsupervised and fast. The algorithm is compared to other conventional methods using several simulated data sets whose characteristics closely resemble those of in vivo recordings. For these data sets, we found that the proposed algorithm outperformed conventional methods.
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              Measuring phase-amplitude coupling between neuronal oscillations of different frequencies.

              Neuronal oscillations of different frequencies can interact in several ways. There has been particular interest in the modulation of the amplitude of high-frequency oscillations by the phase of low-frequency oscillations, since recent evidence suggests a functional role for this type of cross-frequency coupling (CFC). Phase-amplitude coupling has been reported in continuous electrophysiological signals obtained from the brain at both local and macroscopic levels. In the present work, we present a new measure for assessing phase-amplitude CFC. This measure is defined as an adaptation of the Kullback-Leibler distance-a function that is used to infer the distance between two distributions-and calculates how much an empirical amplitude distribution-like function over phase bins deviates from the uniform distribution. We show that a CFC measure defined this way is well suited for assessing the intensity of phase-amplitude coupling. We also review seven other CFC measures; we show that, by some performance benchmarks, our measure is especially attractive for this task. We also discuss some technical aspects related to the measure, such as the length of the epochs used for these analyses and the utility of surrogate control analyses. Finally, we apply the measure and a related CFC tool to actual hippocampal recordings obtained from freely moving rats and show, for the first time, that the CA3 and CA1 regions present different CFC characteristics.
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                Author and article information

                Contributors
                sanja.mikulovic@neuro.uu.se
                richardson.leao@neuro.uu.se
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                7 September 2018
                7 September 2018
                2018
                : 9
                : 3638
                Affiliations
                [1 ]ISNI 0000 0004 1936 9457, GRID grid.8993.b, Developmental Genetics, Department of Neuroscience, , Uppsala University, ; Husarg 3, Uppsala, 75234 Sweden
                [2 ]ISNI 0000 0004 1936 9457, GRID grid.8993.b, Division of Scientific Computing, Department of Information Technology, , Uppsala University, ; Box 337, Uppsala, 75105 Sweden
                [3 ]ISNI 0000 0000 9687 399X, GRID grid.411233.6, Brain Institute, , Federal University of Rio Grande do Norte, ; Av. Nascimento de Castro 2155, Natal, RN 59056-450 Brazil
                Author information
                http://orcid.org/0000-0002-9877-7816
                http://orcid.org/0000-0001-6418-5460
                http://orcid.org/0000-0001-8496-1965
                Article
                5907
                10.1038/s41467-018-05907-w
                6128904
                30194386
                5b467777-efd3-44ab-8c79-0847b4239362
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 1 April 2018
                : 31 July 2018
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