The Temporal Association Cortex Plays a Key Role in Auditory-Driven Maternal Plasticity

Gen ichi Tasaka; Libi Feigin; Ido Maor; Maya Groysman; Laura A. DeNardo; Jennifer K. Schiavo; Robert C. Froemke; Liqun Luo; Adi Mizrahi

doi:10.1016/j.neuron.2020.05.004

The Temporal Association Cortex Plays a Key Role in Auditory-Driven Maternal Plasticity

Gen ichi Tasaka, Libi Feigin, Ido Maor, Maya Groysman, Laura A. DeNardo, Jennifer K. Schiavo, Robert C. Froemke, Liqun Luo, Adi Mizrahi^*

^*Corresponding author for this work

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

46 Scopus citations

Abstract

Mother-infant bonding develops rapidly following parturition and is accompanied by changes in sensory perception and behavior. Here, we study how ultrasonic vocalizations (USVs) are represented in the brain of mothers. Using a mouse line that allows temporally controlled genetic access to active neurons, we find that the temporal association cortex (TeA) in mothers exhibits robust USV responses. Rabies tracing from USV-responsive neurons reveals extensive subcortical and cortical inputs into TeA. A particularly dominant cortical source of inputs is the primary auditory cortex (A1), suggesting strong A1-to-TeA connectivity. Chemogenetic silencing of USV-responsive neurons in TeA impairs auditory-driven maternal preference in a pup-retrieval assay. Furthermore, dense extracellular recordings from awake mice reveal changes of both single-neuron and population responses to USVs in TeA, improving discriminability of pup calls in mothers compared with naive females. These data indicate that TeA plays a key role in encoding and perceiving pup cries during motherhood.

Original language	American English
Pages (from-to)	566-579.e7
Journal	Neuron
Volume	107
Issue number	3
DOIs	https://doi.org/10.1016/j.neuron.2020.05.004
State	Published - 5 Aug 2020

Bibliographical note

Funding Information:
We thank members of the Mizrahi laboratories for comments on the manuscript and Yonatan Loewenstein and Israel Nelken for advice on statistics. We thank the Gatsby Foundation for partnering in the development of neuropixels and providing access to engineering prototype probes. We thank HHMI Janelia and UCL for helpful discussion, the development of data acquisition and analysis tools, and training in the use of Neuropixels. We gratefully acknowledge the support of the NVIDIA Corporation with the donation of the Titan Xp graphics processing unit (GPU) used for this research and the analysis of Neuropixels data. This work was supported by an ERC grant to A.M. ( 616063 ); an Israel Science Foundation (ISF) grant to A.M. ( 224/17 ); a Howard Hughes Institute Collaborative Award; a US-Israel Bi-national grant ( NSF grant BRAIN EAGER ) to L.L. and A.M.; and an NIH grant to L.L. ( R01-NS050580 ). G.T. was supported by a postdoctoral fellowship from the Uehara Memorial Foundation and the Edmond and Lily Safra Center for Brain Sciences .

Funding Information:
We thank members of the Mizrahi laboratories for comments on the manuscript and Yonatan Loewenstein and Israel Nelken for advice on statistics. We thank the Gatsby Foundation for partnering in the development of neuropixels and providing access to engineering prototype probes. We thank HHMI Janelia and UCL for helpful discussion, the development of data acquisition and analysis tools, and training in the use of Neuropixels. We gratefully acknowledge the support of the NVIDIA Corporation with the donation of the Titan Xp graphics processing unit (GPU) used for this research and the analysis of Neuropixels data. This work was supported by an ERC grant to A.M. (616063); an Israel Science Foundation (ISF) grant to A.M. (224/17); a Howard Hughes Institute Collaborative Award; a US-Israel Bi-national grant (NSF grant BRAIN EAGER) to L.L. and A.M.; and an NIH grant to L.L. (R01-NS050580). G.T. was supported by a postdoctoral fellowship from the Uehara Memorial Foundation and the Edmond and Lily Safra Center for Brain Sciences. G.T. and A.M. designed experiments. L.L. and L.A.D. contributed TRAP2 mice prior to publication and provided advice. R.C.F. and J.K.S. designed the auditory-driven maternal behavior experiment. M.G. made the adeno-associated viruses. L.F. conducted the Neuropixels experiment and analyzed the data. I.M. contributed to the Neuropixels experiment. G.T. conducted all experiments and analyzed the data. G.T. and A.M. wrote the paper, with input from all authors. The authors declare no competing interests.

Publisher Copyright:
© 2020 Elsevier Inc.

Keywords

TRAP
auditory cortex
motherhood
neuropixels
plasticity
rabies tracing
temporal association cortex
ultra sonic vocalizations

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10.1016/j.neuron.2020.05.004

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title = "The Temporal Association Cortex Plays a Key Role in Auditory-Driven Maternal Plasticity",

abstract = "Mother-infant bonding develops rapidly following parturition and is accompanied by changes in sensory perception and behavior. Here, we study how ultrasonic vocalizations (USVs) are represented in the brain of mothers. Using a mouse line that allows temporally controlled genetic access to active neurons, we find that the temporal association cortex (TeA) in mothers exhibits robust USV responses. Rabies tracing from USV-responsive neurons reveals extensive subcortical and cortical inputs into TeA. A particularly dominant cortical source of inputs is the primary auditory cortex (A1), suggesting strong A1-to-TeA connectivity. Chemogenetic silencing of USV-responsive neurons in TeA impairs auditory-driven maternal preference in a pup-retrieval assay. Furthermore, dense extracellular recordings from awake mice reveal changes of both single-neuron and population responses to USVs in TeA, improving discriminability of pup calls in mothers compared with naive females. These data indicate that TeA plays a key role in encoding and perceiving pup cries during motherhood.",

keywords = "TRAP, auditory cortex, motherhood, neuropixels, plasticity, rabies tracing, temporal association cortex, ultra sonic vocalizations",

author = "Tasaka, {Gen ichi} and Libi Feigin and Ido Maor and Maya Groysman and DeNardo, {Laura A.} and Schiavo, {Jennifer K.} and Froemke, {Robert C.} and Liqun Luo and Adi Mizrahi",

note = "Funding Information: We thank members of the Mizrahi laboratories for comments on the manuscript and Yonatan Loewenstein and Israel Nelken for advice on statistics. We thank the Gatsby Foundation for partnering in the development of neuropixels and providing access to engineering prototype probes. We thank HHMI Janelia and UCL for helpful discussion, the development of data acquisition and analysis tools, and training in the use of Neuropixels. We gratefully acknowledge the support of the NVIDIA Corporation with the donation of the Titan Xp graphics processing unit (GPU) used for this research and the analysis of Neuropixels data. This work was supported by an ERC grant to A.M. ( 616063 ); an Israel Science Foundation (ISF) grant to A.M. ( 224/17 ); a Howard Hughes Institute Collaborative Award; a US-Israel Bi-national grant ( NSF grant BRAIN EAGER ) to L.L. and A.M.; and an NIH grant to L.L. ( R01-NS050580 ). G.T. was supported by a postdoctoral fellowship from the Uehara Memorial Foundation and the Edmond and Lily Safra Center for Brain Sciences . Funding Information: We thank members of the Mizrahi laboratories for comments on the manuscript and Yonatan Loewenstein and Israel Nelken for advice on statistics. We thank the Gatsby Foundation for partnering in the development of neuropixels and providing access to engineering prototype probes. We thank HHMI Janelia and UCL for helpful discussion, the development of data acquisition and analysis tools, and training in the use of Neuropixels. We gratefully acknowledge the support of the NVIDIA Corporation with the donation of the Titan Xp graphics processing unit (GPU) used for this research and the analysis of Neuropixels data. This work was supported by an ERC grant to A.M. (616063); an Israel Science Foundation (ISF) grant to A.M. (224/17); a Howard Hughes Institute Collaborative Award; a US-Israel Bi-national grant (NSF grant BRAIN EAGER) to L.L. and A.M.; and an NIH grant to L.L. (R01-NS050580). G.T. was supported by a postdoctoral fellowship from the Uehara Memorial Foundation and the Edmond and Lily Safra Center for Brain Sciences. G.T. and A.M. designed experiments. L.L. and L.A.D. contributed TRAP2 mice prior to publication and provided advice. R.C.F. and J.K.S. designed the auditory-driven maternal behavior experiment. M.G. made the adeno-associated viruses. L.F. conducted the Neuropixels experiment and analyzed the data. I.M. contributed to the Neuropixels experiment. G.T. conducted all experiments and analyzed the data. G.T. and A.M. wrote the paper, with input from all authors. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

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The Temporal Association Cortex Plays a Key Role in Auditory-Driven Maternal Plasticity

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Keywords

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