Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells

Sang Hun Lee; Ivan Marchionni; Marianne Bezaire; Csaba Varga; Nathan Danielson; Matthew Lovett-Barron; Attila Losonczy; Ivan Soltesz

doi:10.1016/j.neuron.2014.03.034

Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells

Sang Hun Lee
, Ivan Marchionni
, Marianne Bezaire
, Csaba Varga
, Nathan Danielson
, Matthew Lovett-Barron
, Attila Losonczy
, Ivan Soltesz

Neuroscience

Producción científica: Article › revisión exhaustiva

267 Citas (Scopus)

Resumen

CA1 pyramidal cells (PCs) are not homogeneous but rather can be grouped by molecular, morphological, and functional properties. However, less is known about synaptic sources differentiating PCs. Using paired recordings invitro, two-photon Ca²⁺ imaging invivo, and computational modeling, we found thatparvalbumin-expressing basket cells (PVBCs) evoked greater inhibition in CA1 PCs located in the deep compared to superficial layer of stratum pyramidale. In turn, analysis of reciprocal connectivity revealed more frequent excitatory inputs to PVBCs bysuperficial PCs, demonstrating bias in target selection by both the excitatory and inhibitory local connections in CA1. Additionally, PVBCs further segregated among deep PCs, preferentially innervating the amygdala-projecting PCs but receiving preferential excitation from the prefrontal cortex-projecting PCs, thus revealing distinct perisomatic inhibitory interactions between separate output channels. These results demonstrate the presence of heterogeneous PVBC-PC microcircuits, potentially contributing to the sparse and distributed structure of hippocampal network activity.

Idioma original	English
Páginas (desde-hasta)	1129-1144
Número de páginas	16
Publicación	Neuron
Volumen	82
N.º	5
DOI	https://doi.org/10.1016/j.neuron.2014.03.034
Estado	Published - jun 4 2014

Nota bibliográfica

Funding Information:
We thank R. Zhu, J. Varga, O. Rodriguez, M.K. Oberoi, A. Sharma, P. Kaifosh, A. Castro, and J. Zaremba for technical support, D.C. Lyon for assistance with Neurolucida System, and E. Krook-Magnuson, H. Kim, M. Maroso, Y.J. Kang, and C. Krook-Magnuson for generous advice. This work was supported by the U.S. National Institutes of Health (NS74432 to I.S.), National Science Foundation (DGE-0808392 to M.B.), University of California Irvine Center for Autism Research and Treatment (to I.S.), by Searle, Human Frontiers Science Program, McKnight Memory and Cognitive Disorders Award, and Harvey L. Karp Discovery Award (to A.L.), and NSERC postgraduate scholarship (to M.L.-B.). Computer modeling was supported by NSF’s XSEDE program through the Neuroscience Gateway Portal for computational neuroscientists and via XSEDE Startup Allocations (TG-IBN100011 to M.B. and TG-IBN130022 to I.S.). Technical support and parallel computing time were provided by the San Diego Supercomputing Center’s Trestles computer, the University of Texas’ Stampede computer, and the University of California Irvine’s High Performance Computer.

Financiación

We thank R. Zhu, J. Varga, O. Rodriguez, M.K. Oberoi, A. Sharma, P. Kaifosh, A. Castro, and J. Zaremba for technical support, D.C. Lyon for assistance with Neurolucida System, and E. Krook-Magnuson, H. Kim, M. Maroso, Y.J. Kang, and C. Krook-Magnuson for generous advice. This work was supported by the U.S. National Institutes of Health (NS74432 to I.S.), National Science Foundation (DGE-0808392 to M.B.), University of California Irvine Center for Autism Research and Treatment (to I.S.), by Searle, Human Frontiers Science Program, McKnight Memory and Cognitive Disorders Award, and Harvey L. Karp Discovery Award (to A.L.), and NSERC postgraduate scholarship (to M.L.-B.). Computer modeling was supported by NSF\u2019s XSEDE program through the Neuroscience Gateway Portal for computational neuroscientists and via XSEDE Startup Allocations (TG-IBN100011 to M.B. and TG-IBN130022 to I.S.). Technical support and parallel computing time were provided by the San Diego Supercomputing Center\u2019s Trestles computer, the University of Texas\u2019 Stampede computer, and the University of California Irvine\u2019s High Performance Computer.

Financiadores	Número del financiador
Searle, Human Frontiers Science Program
McKnight Foundation
University of California Irvine Center for Autism Research and Treatment
National Institutes of Health (NIH)
Natural Sciences and Engineering Research Council of Canada
U.S. Department of Energy Chinese Academy of Sciences Guangzhou Municipal Science and Technology Project Oak Ridge National Laboratory Extreme Science and Engineering Discovery Environment National Science Foundation National Energy Research Scientific Computing Center National Natural Science Foundation of China	TG-IBN130022, TG-IBN100011, DGE-0808392
Institute of Neurological Disorders and Stroke National Advisory Neurological Disorders and Stroke Council	R01NS074432

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2014.03.034

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title = "Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells",

abstract = "CA1 pyramidal cells (PCs) are not homogeneous but rather can be grouped by molecular, morphological, and functional properties. However, less is known about synaptic sources differentiating PCs. Using paired recordings invitro, two-photon Ca2+ imaging invivo, and computational modeling, we found thatparvalbumin-expressing basket cells (PVBCs) evoked greater inhibition in CA1 PCs located in the deep compared to superficial layer of stratum pyramidale. In turn, analysis of reciprocal connectivity revealed more frequent excitatory inputs to PVBCs bysuperficial PCs, demonstrating bias in target selection by both the excitatory and inhibitory local connections in CA1. Additionally, PVBCs further segregated among deep PCs, preferentially innervating the amygdala-projecting PCs but receiving preferential excitation from the prefrontal cortex-projecting PCs, thus revealing distinct perisomatic inhibitory interactions between separate output channels. These results demonstrate the presence of heterogeneous PVBC-PC microcircuits, potentially contributing to the sparse and distributed structure of hippocampal network activity.",

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AU - Marchionni, Ivan

AU - Bezaire, Marianne

AU - Varga, Csaba

AU - Danielson, Nathan

AU - Lovett-Barron, Matthew

AU - Losonczy, Attila

AU - Soltesz, Ivan

N1 - Funding Information: We thank R. Zhu, J. Varga, O. Rodriguez, M.K. Oberoi, A. Sharma, P. Kaifosh, A. Castro, and J. Zaremba for technical support, D.C. Lyon for assistance with Neurolucida System, and E. Krook-Magnuson, H. Kim, M. Maroso, Y.J. Kang, and C. Krook-Magnuson for generous advice. This work was supported by the U.S. National Institutes of Health (NS74432 to I.S.), National Science Foundation (DGE-0808392 to M.B.), University of California Irvine Center for Autism Research and Treatment (to I.S.), by Searle, Human Frontiers Science Program, McKnight Memory and Cognitive Disorders Award, and Harvey L. Karp Discovery Award (to A.L.), and NSERC postgraduate scholarship (to M.L.-B.). Computer modeling was supported by NSF’s XSEDE program through the Neuroscience Gateway Portal for computational neuroscientists and via XSEDE Startup Allocations (TG-IBN100011 to M.B. and TG-IBN130022 to I.S.). Technical support and parallel computing time were provided by the San Diego Supercomputing Center’s Trestles computer, the University of Texas’ Stampede computer, and the University of California Irvine’s High Performance Computer.

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JF - Neuron

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ER -

Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells

Resumen

Nota bibliográfica

Financiación

ASJC Scopus subject areas

Acceder al documento

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Huella

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