Inhibitory Plasticity Permits the Recruitment of CA2 Pyramidal Neurons by CA3

Nasrallah, Kaoutsar; Piskorowski, Rebecca A.; Chevaleyre, Vivien

doi:10.1523/eneuro.0049-15.2015

Cited by 43 publications

(68 citation statements)

References 31 publications

(56 reference statements)

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“…We have recently shown that a HFS in SR induces an iLTD in area CA2 that results in a large increase in the depolarizing component of the PSP amplitude evoked by SC stimulation (Nasrallah et al, 2015). We asked whether the plasticity of inhibitory transmission that we can induce with a distal input HFS could be sufficient to modulate the level of excitatory drive at SLM-CA2 synapses.…”

Section: Hfs In Slm Induces Iltd and Alters The Excitatory/inhibitorymentioning

confidence: 97%

“…We have recently shown that inhibitory synapses recruited in SLM express an activity-dependent hetero-synaptic LTD following HFS of proximal inputs (Nasrallah et al, 2015). We investigated whether iLTD of distal CA2 inputs could also be induced homo-synapticaly by HFS in SLM.…”

Section: Hfs In Slm Induces Iltd and Alters The Excitatory/inhibitorymentioning

confidence: 99%

“…In area CA2, a HFS of proximal SC inputs can trigger a heterosynaptic iLTD of distally evoked IPSCs and a hetero-synaptic disinhibition of distal excitatory inputs (Nasrallah et al, 2015). Could this interplay be bi-directional?…”

Section: Stimulation In Slm Induces a Hetero-synaptic Iltd And Increamentioning

confidence: 99%

“…In contrast to SC-CA2 excitatory synapses, inhibitory transmission from parvalbumin-expressing (PV+) interneurons in area CA2 is highly plastic, undergoing a long-term depression (iLTD) that is mediated by delta opioid receptor (DOR) activation following stimulation of SC inputs or activation of DORs with agonist application (Piskorowski & Chevaleyre, 2013). This DOR-mediated iLTD allows a lasting increase of both proximal and distal input excitatory drive onto CA2 PNs (Nasrallah, Piskorowski, & Chevaleyre, 2015). Therefore, we wondered whether the crosstalk between proximal and distal inputs could be bi-directional, i.e.…”

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Bi-directional interplay between proximal and distal inputs to CA2 pyramidal neurons

Nasrallah

Piskorowski

Chevaleyre

2017

Neurobiology of Learning and Memory

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Section: Hfs In Slm Induces Iltd and Alters The Excitatory/inhibitorymentioning

confidence: 97%

Section: Hfs In Slm Induces Iltd and Alters The Excitatory/inhibitorymentioning

confidence: 99%

Section: Stimulation In Slm Induces a Hetero-synaptic Iltd And Increamentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Bi-directional interplay between proximal and distal inputs to CA2 pyramidal neurons

Nasrallah

Piskorowski

Chevaleyre

2017

Neurobiology of Learning and Memory

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“…More recently, feedforward recruitment of CA2 inhibitory interneurons was identified to underpin this "delay-relay." Furthermore, longterm depression of the excitation of CA2 inhibitory interneurons permitted distal excitation of CA2 pyramidal neurons, allowing them to fire and relay activity to CA1 (Nasrallah et al 2015). The significance of CA2 and its connections was recently highlighted as critical for social memory (Hitti and Siegelbaum 2014;Stevenson and Caldwell 2014) and in a mouse model of schizophrenia where CA2 is functionally disconnected from the trisynaptic pathway by excessive feedforward inhibition (Piskorowski et al 2016).…”

Section: Circuit-level Voltage Imaging Approachesmentioning

confidence: 99%

Voltage imaging to understand connections and functions of neuronal circuits

Antic

Empson

Knöpfel

2016

Journal of Neurophysiology

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Antic SD, Empson RM, Knöpfel T. Voltage imaging to understand connections and functions of neuronal circuits. J Neurophysiol 116: 135-152, 2016. First published April 13, 2016 doi:10.1152/jn.00226.2016.-Understanding of the cellular mechanisms underlying brain functions such as cognition and emotions requires monitoring of membrane voltage at the cellular, circuit, and system levels. Seminal voltage-sensitive dye and calcium-sensitive dye imaging studies have demonstrated parallel detection of electrical activity across populations of interconnected neurons in a variety of preparations. A game-changing advance made in recent years has been the conceptualization and development of optogenetic tools, including genetically encoded indicators of voltage (GEVIs) or calcium (GECIs) and genetically encoded light-gated ion channels (actuators, e.g., channelrhodopsin2). Compared with low-molecular-weight calcium and voltage indicators (dyes), the optogenetic imaging approaches are 1) cell type specific, 2) less invasive, 3) able to relate activity and anatomy, and 4) facilitate long-term recordings of individual cells' activities over weeks, thereby allowing direct monitoring of the emergence of learned behaviors and underlying circuit mechanisms. We highlight the potential of novel approaches based on GEVIs and compare those to calcium imaging approaches. We also discuss how novel approaches based on GEVIs (and GECIs) coupled with genetically encoded actuators will promote progress in our knowledge of brain circuits and systems.GECI; GEVI; membrane voltage; neurophysiology; optical imaging THE IMPORTANCE OF STUDYING VOLTAGE SIGNALS within biological organisms was realized as far back as the eighteenth century by the scientist Luigi Galvani (1737-1798). Galvani proposed that electrical forces power movement in animals, which he termed "animal electricity"; thus all life is electrical (Bresadola 2008). Galvani's seminal work inspired the invention by Alessandro Volta of the first electric battery, used by Michael Faraday and other pioneers of physics. In a straightforward manner, biology gave birth to the modern physics of electricity and electronic circuits. This enormous contribution of biology to the modern world is often overlooked.Electrophysiological measures, instigated by Galvani, Volta, Helmholtz, Bernstein, Adrian, Renshaw, Curtis, Cole, Hodgkin, Huxley, and others, have become a key methodology in neuroscience because fluctuations of membrane potential both are the physical means of signal transmission among the elements of a neuronal circuit and comprise the substrate of fast information processing (integration) in the brain. It is therefore indubitable that detecting and recording voltage changes from neurons in living animals and linking these signals to cognitive and emotional tasks is required for understanding the mammalian brain. In this review we explore the idea that the brain is essentially an electric information processing device with simultaneous multisite processing and that, consequently, simult...

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Diversity of dendritic morphology and entorhinal cortex synaptic effectiveness in mouse CA2 pyramidal neurons

et al. 2018

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Excitatory synaptic inputs from specific brain regions are often targeted to distinct dendritic arbors on hippocampal pyramidal neurons. Recent work has suggested that CA2 pyramidal neurons respond robustly and preferentially to excitatory input into the stratum lacunosum moleculare (SLM), with a relatively modest response to Schaffer collateral excitatory input into stratum radiatum (SR) in acute mouse hippocampal slices, but the extent to which this difference may be explained by morphology is unknown. In an effort to replicate these findings and to better understand the role of dendritic morphology in shaping responses from proximal and distal synaptic sites, we measured excitatory postsynaptic currents and action potentials in CA2 pyramidal cells in response to SR and SLM stimulation and subsequently analyzed confocal images of the filled cells. We found that, in contrast to previous reports, SR stimulation evoked substantial responses in all recorded CA2 pyramidal cells. Strikingly, however, we found that not all neurons responded to SLM stimulation, and in those neurons that did, responses evoked by SLM and SR were comparable in size and effectiveness in inducing action potentials. In a comprehensive morphometric analysis of CA2 pyramidal cell apical dendrites, we found that the neurons that were unresponsive to SLM stimulation were the same ones that lacked substantial apical dendritic arborization in the SLM. Neurons responsive to both SR and SLM stimulation had roughly equal amounts of dendritic branching in each layer. Remarkably, our study in mouse CA2 generally replicates the work characterizing the diversity of CA2 pyramidal cells in the guinea pig hippocampus. We conclude, then, that like in guinea pig, mouse CA2 pyramidal cells have a diverse apical dendrite morphology that is likely to be reflective of both the amount and source of excitatory input into CA2 from the entorhinal cortex and CA3.

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Inhibitory Plasticity Permits the Recruitment of CA2 Pyramidal Neurons by CA3

Cited by 43 publications

References 31 publications

Bi-directional interplay between proximal and distal inputs to CA2 pyramidal neurons

Bi-directional interplay between proximal and distal inputs to CA2 pyramidal neurons

Voltage imaging to understand connections and functions of neuronal circuits

Diversity of dendritic morphology and entorhinal cortex synaptic effectiveness in mouse CA2 pyramidal neurons

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