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Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type- Dependent Monosynaptic Tracing

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Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type- Dependent Monosynaptic Tracing This Accepted Manuscript has not been copyedited and formatted. The final version may differ from this version. Research Articles: Systems/Circuits Neuronal organization in the inferior colliculus revisited with cell-type- dependent monosynaptic tracing Chenggang Chen1, Mingxiu Cheng1,2, Tetsufumi Ito3 and Sen Song1 1Tsinghua Laboratory of Brain and Intelligence (THBI) and Department of Biomedical Engineering, Beijing Innovation Center for Future Chip, Center for Brain-Inspired Computing Research, McGovern Institute for Brain Research, Tsinghua University, Beijing, 100084, China 2National Institute of Biological Sciences, Beijing, 102206, China 3Anatomy II, School of Medicine, Kanazawa Medical University, Uchinada, Ishikawa, 920-0293, Japan DOI: 10.1523/JNEUROSCI.2173-17.2018 Received: 31 July 2017 Revised: 2 February 2018 Accepted: 7 February 2018 Published: 24 February 2018 Author contributions: C.C., T.I., and S.S. designed research; C.C. and M.C. performed research; C.C. and T.I. analyzed data; C.C. wrote the first draft of the paper; C.C., T.I., and S.S. edited the paper; C.C., T.I., and S.S. wrote the paper. Conflict of Interest: The authors declare no competing financial interests. This work was supported by funding from the National Natural Science Foundation of China (31571095, 91332122, for S.S.), Special Fund of Suzhou-Tsinghua Innovation Leading Action (for S.S.), Beijing Program on the Study of Brain-Inspired Computing System and Related Core Technologies (for S.S.), Beijing Innovation Center for Future Chip (for S.S.), and Chinese Academy of Sciences Institute of Psychology Key Laboratory of Mental Health Open Research Grant (KLMH2012K02, for S.S.), grants from Ministry of Education, Science, and Culture of Japan (KAKENHI grant, Grant numbers 16K07026 and 16H01501; for T.I.), and Takahashi Industrial and Economic Research Foundation (for T.I.). We thank D. Cai for technical assistance and L. Shen, K. Yuan, X. Wang and D. Oliver for comments on the manuscript. Corresponding authors: Sen Song (Lead), Tsinghua University, Beijing, 100084, China, E-mail: [email protected]; Tetsufumi Ito, Kanazawa Medical University, Uchinada, Ishikawa, 920-0293, Japan, E-mail: [email protected] Cite as: J. Neurosci ; 10.1523/JNEUROSCI.2173-17.2018 Alerts: Sign up at www.jneurosci.org/cgi/alerts to receive customized email alerts when the fully formatted version of this article is published. Accepted manuscripts are peer-reviewed but have not been through the copyediting, formatting, or proofreading process. Copyright © 2018 the authors 1 Title: 2 Neuronal organization in the inferior colliculus revisited with cell-type-dependent monosynaptic 3 tracing 4 Abbreviated title: 5 Neuronal organization in the inferior colliculus 6 Authors: 7 Chenggang Chen (ORCID ID: 0000-0003-4143-2427) 1, Mingxiu Cheng (ORCID ID: 8 0000-0003-1957-623X) 1, 2, Tetsufumi Ito (ORCID ID: 0000-0003-4516-9283) 3, Sen Song 9 (ORCID ID: 0000-0001-5587-0730) 1 10 Affiliations: 11 1Tsinghua Laboratory of Brain and Intelligence (THBI) and Department of Biomedical 12 Engineering, Beijing Innovation Center for Future Chip, Center for Brain-Inspired Computing 13 Research, McGovern Institute for Brain Research, Tsinghua University, Beijing, 100084, China; 14 2National Institute of Biological Sciences, Beijing, 102206, China; 15 3Anatomy II, School of Medicine, Kanazawa Medical University, Uchinada, Ishikawa, 920-0293, 16 Japan; 17 Corresponding authors: 18 Sen Song (Lead) 19 Tsinghua University, Beijing, 100084, China 20 E-mail: [email protected] 21 Tetsufumi Ito 22 Kanazawa Medical University, Uchinada, Ishikawa, 920-0293, Japan 23 E-mail: [email protected] 24 Pages: 37 Figures: 9 Tables: 1 25 Abstract: 250 Significance Statement: 116 Introduction: 657 Discussion: 1530 26 Conflicts of interest 27 The authors declare no competing financial interests. 28 Acknowledgments 29 This work was supported by funding from the National Natural Science Foundation of China 30 (31571095, 91332122, for S.S.), Special Fund of Suzhou-Tsinghua Innovation Leading Action (for 31 S.S.), Beijing Program on the Study of Brain-Inspired Computing System and Related Core 32 Technologies (for S.S.), Beijing Innovation Center for Future Chip (for S.S.), and Chinese 33 Academy of Sciences Institute of Psychology Key Laboratory of Mental Health Open Research 34 Grant (KLMH2012K02, for S.S.), grants from Ministry of Education, Science, and Culture of 35 Japan (KAKENHI grant, Grant numbers 16K07026 and 16H01501; for T.I.), and Takahashi 36 Industrial and Economic Research Foundation (for T.I.). We thank D. Cai for technical assistance 37 and L. Shen, K. Yuan, X. Wang and D. Oliver for comments on the manuscript. 1 38 Abstract 39 The inferior colliculus (IC) is a critical integration center in the auditory pathway. However, since 40 the inputs to the IC have typically been studied by the use of conventional anterograde and 41 retrograde tracers, the neuronal organization and cell-type-specific connections in the IC are 42 poorly understood. Here, we utilized monosynaptic rabies tracing and in situ hybridization 43 combined with excitatory and inhibitory Cre transgenic mouse lines of both sexes to characterize 44 the brain-wide and cell-type-specific inputs to specific neuron types within the lemniscal IC core 45 and nonlemniscal IC shell. We observed that both excitatory and inhibitory neurons of the IC shell 46 predominantly received ascending inputs rather than descending or core inputs. Correlation and 47 clustering analyses revealed two groups of excitatory neurons in the shell: one received inputs 48 from a combination of ascending nuclei, and the other received inputs from a combination of 49 descending nuclei, neuromodulatory nuclei and the contralateral IC. In contrast, inhibitory neurons 50 in the core received inputs from the same combination of all nuclei. After normalizing the 51 extrinsic inputs, we found that core inhibitory neurons received a higher proportion of inhibitory 52 inputs from the ventral nucleus of the lateral lemniscus than excitatory neurons. Furthermore, the 53 inhibitory neurons preferentially received inhibitory inputs from the contralateral IC shell. Since 54 IC inhibitory neurons innervate the thalamus and contralateral IC, the inhibitory inputs we 55 uncovered here suggest two long-range disinhibitory circuits. In summary, we found: (1) dominant 56 ascending inputs to the shell; (2) two subpopulations of shell excitatory neurons; and (3) two 57 disinhibitory circuits. 58 2 59 Significance Statement 60 Sound undergoes extensive processing in the brainstem. The inferior colliculus (IC) core is 61 classically viewed as the integration center for ascending auditory information, whereas the IC 62 shell integrates descending feedback information. Here, we demonstrate that ascending inputs 63 predominated in the IC shell but appeared to be separated from the descending inputs. The 64 presence of inhibitory projection neurons is a unique feature of the auditory ascending pathways, 65 but the connections of these neurons are poorly understood. Interestingly, we also found that 66 inhibitory neurons in the IC core and shell preferentially received inhibitory inputs from ascending 67 nuclei and contralateral IC, respectively. Therefore, our results suggest a bipartite domain in the IC 68 shell and disinhibitory circuits in the IC. 3 69 Introduction 70 The auditory midbrain or inferior colliculus (IC) is a critical integration center of the auditory 71 pathway and is divided into core (central nucleus) and shell (dorsal and lateral nucleus) 72 subdivisions according to dendritic morphology and axonal trajectories (Oliver and Morest, 1984). 73 The IC core primarily receives ascending brainstem inputs (Cant and Benson, 2006). In contrast, 74 physiological and behavioral studies have demonstrated that the IC shell not only receives 75 ascending inputs (Loftus et al., 2008) but also descending auditory cortex (AC) and IC core inputs 76 (Winer et al., 1998; Winer and Schreiner, 2005). IC shell neurons display broader tuning (Syka et 77 al., 2000) and stronger stimulus-specific adaptation (SSA) (Shen et al., 2015) than core neurons, 78 suggesting an influence of both descending and core inputs. On the other hand, the shell neurons 79 also exhibit short response latencies similar to the IC core neurons (Syka et al., 2000), and shell 80 stimulation directly induces innate auditory behavior (Xiong et al., 2015), implying an effect of 81 brainstem inputs. However, whether the IC shell primarily receives descending and core inputs or 82 ascending inputs is still unclear. 83 The core and shell subdivisions can also be divided into finer units of IC neuronal organization, 84 i.e., synaptic domains, which receive inputs from different combinations of nuclei and are 85 considered to be a fundamental feature of the IC and superior colliculus (SC) (Oliver, 2005). 86 Synaptic domains or functional modules exist in specific locations of the core and shell, exhibit 87 specific monaural, binaural and SSA responses, and receive specific ascending or descending 88 inputs (Loftus et al., 2010; Ayala et al., 2015). However, previous studies only defined the synaptic 89 domains by anterograde or retrograde tracing in terms of their anatomical location and not on a 90 neuronal level. When neurons such as neurons in the deep shell layer (Malmierca et al., 2011) or 4 91 stellate neurons in the core (Oliver, 2005) project dendrites out of a specific location (i.e., injection 92
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