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Research Articles, Systems/Circuits

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

Chenggang Chen, Mingxiu Cheng, Tetsufumi Ito and Sen Song
Journal of Neuroscience 28 March 2018, 38 (13) 3318-3332; DOI: https://doi.org/10.1523/JNEUROSCI.2173-17.2018
Chenggang Chen
1Tsinghua Laboratory of Brain and Intelligence 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,
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Mingxiu Cheng
1Tsinghua Laboratory of Brain and Intelligence 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, and
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Tetsufumi Ito
3Anatomy II, School of Medicine, Kanazawa Medical University, Uchinada, Ishikawa, 920-0293, Japan
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Sen Song
1Tsinghua Laboratory of Brain and Intelligence 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,
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Abstract

The inferior colliculus (IC) is a critical integration center in the auditory pathway. However, because the inputs to the IC have typically been studied by the use of conventional anterograde and retrograde tracers, the neuronal organization and cell-type-specific connections in the IC are poorly understood. Here, we used monosynaptic rabies tracing and in situ hybridization combined with excitatory and inhibitory Cre transgenic mouse lines of both sexes to characterize the brainwide and cell-type-specific inputs to specific neuron types within the lemniscal IC core and nonlemniscal IC shell. We observed that both excitatory and inhibitory neurons of the IC shell predominantly received ascending inputs rather than descending or core inputs. Correlation and clustering analyses revealed two groups of excitatory neurons in the shell: one received inputs from a combination of ascending nuclei, and the other received inputs from a combination of descending nuclei, neuromodulatory nuclei, and the contralateral IC. In contrast, inhibitory neurons in the core received inputs from the same combination of all nuclei. After normalizing the extrinsic inputs, we found that core inhibitory neurons received a higher proportion of inhibitory inputs from the ventral nucleus of the lateral lemniscus than excitatory neurons. Furthermore, the inhibitory neurons preferentially received inhibitory inputs from the contralateral IC shell. Because IC inhibitory neurons innervate the thalamus and contralateral IC, the inhibitory inputs we uncovered here suggest two long-range disinhibitory circuits. In summary, we found: (1) dominant ascending inputs to the shell, (2) two subpopulations of shell excitatory neurons, and (3) two disinhibitory circuits.

SIGNIFICANCE STATEMENT Sound undergoes extensive processing in the brainstem. The inferior colliculus (IC) core is classically viewed as the integration center for ascending auditory information, whereas the IC shell integrates descending feedback information. Here, we demonstrate that ascending inputs predominated in the IC shell but appeared to be separated from the descending inputs. The presence of inhibitory projection neurons is a unique feature of the auditory ascending pathways, but the connections of these neurons are poorly understood. Interestingly, we also found that inhibitory neurons in the IC core and shell preferentially received inhibitory inputs from ascending nuclei and contralateral IC, respectively. Therefore, our results suggest a bipartite domain in the IC shell and disinhibitory circuits in the IC.

  • in situ hybridization
  • inferior colliculus
  • rabies virus
  • transgenic mice
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The Journal of Neuroscience: 38 (13)
Journal of Neuroscience
Vol. 38, Issue 13
28 Mar 2018
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Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type-Dependent Monosynaptic Tracing
Chenggang Chen, Mingxiu Cheng, Tetsufumi Ito, Sen Song
Journal of Neuroscience 28 March 2018, 38 (13) 3318-3332; DOI: 10.1523/JNEUROSCI.2173-17.2018

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Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type-Dependent Monosynaptic Tracing
Chenggang Chen, Mingxiu Cheng, Tetsufumi Ito, Sen Song
Journal of Neuroscience 28 March 2018, 38 (13) 3318-3332; DOI: 10.1523/JNEUROSCI.2173-17.2018
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Keywords

  • in situ hybridization
  • inferior colliculus
  • rabies virus
  • transgenic mice

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