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

Research output: Contribution to journal › Article › peer-review

235 Scopus citations

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.

Original language	English
Pages (from-to)	1129-1144
Number of pages	16
Journal	Neuron
Volume	82
Issue number	5
DOIs	https://doi.org/10.1016/j.neuron.2014.03.034
State	Published - Jun 4 2014

Bibliographical note

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.

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2014.03.034

Cite this

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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.",

author = "Lee, {Sang Hun} and Ivan Marchionni and Marianne Bezaire and Csaba Varga and Nathan Danielson and Matthew Lovett-Barron and Attila Losonczy and Ivan Soltesz",

note = "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{\textquoteright}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{\textquoteright}s Trestles computer, the University of Texas{\textquoteright} Stampede computer, and the University of California Irvine{\textquoteright}s High Performance Computer. ",

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doi = "10.1016/j.neuron.2014.03.034",

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AU - Lee, Sang Hun

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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N2 - 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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ER -

Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells

Abstract

Bibliographical note

ASJC Scopus subject areas

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