Differential cell-type dependent brain state modulations of sensory representations in the non-lemniscal mouse inferior colliculus

Chenggang Chen,Sen Song

doi:10.1038/s42003-019-0602-4

Chenggang Chen, Sen Song

Open Access

https://doi.org/10.1038/s42003-019-0602-4

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Abstract

Sensory responses of the neocortex are strongly influenced by brain state changes. However, it remains unclear whether and how the sensory responses of the midbrain are affected. Here we addressed this issue by using in vivo two-photon calcium imaging to monitor the spontaneous and sound-evoked activities in the mouse inferior colliculus (IC). We developed a method enabling us to image the first layer of non-lemniscal IC (IC shell L1) in awake behaving mice. Compared with the awake state, spectral tuning selectivity of excitatory neurons was decreased during isoflurane anesthesia. Calcium imaging in behaving animals revealed that activities of inhibitory neurons were highly correlated with locomotion. Compared with stationary periods, spectral tuning selectivity of excitatory neurons was increased during locomotion. Taken together, our studies reveal that neuronal activities in the IC shell L1 are brain state dependent, whereas the brain state modulates the excitatory and inhibitory neurons differentially.

Highlights

Sensory responses of the neocortex are strongly influenced by brain state changes
In the auditory cortex (ACx), Zhou et al found that the excitatory and parvalbumin-positive inhibitory neurons are inhibited by the cortical layer 1 (L1) neurons, while Schneider et al.[23] reported that inhibitory neurons are excited by motor cortex, which in turn inhibits the excitatory neurons
We found that wakefulness increased the spectral and temporal tuning selectivity of excitatory neurons compared to those measured under anesthesia

Summary

Results

Calcium imaging in the IC shell L1 of behaving mice. To prevent the tissue regrowth and brain movement during awake recordings, we developed to our knowledge a novel method that enabled us to image the IC shell L1 in the awake, behaving mice (Fig. 1a). To compare the spectral tuning selectivity of excitatory and inhibitory neurons during wakefulness and anesthesia, we used pure tone stimuli with different frequencies and intensities to construct the frequency response area (FRA; Fig. 2e, g). To compare the temporal tuning selectivity of excitatory and inhibitory neurons under wakefulness versus anesthesia, we used the click train stimuli with ten different modulation frequencies (Fig. 3a). We compared the temporal tuning half-width and area of excitatory neurons during wakefulness versus urethane anesthesia (Fig. 3e). The temporal tuning selectivity of excitatory neurons under wakefulness was significantly higher than those under urethane anesthesia (area, urethane: 4.9458 ± 0.0126, awake: 4.1378 ± 0.0080; half-width, urethane: 3.8080 ± 0.0145, awake: 3.2778 ± 0.0122; Mann–Whitney U test). Under the urethane anesthesia, tuning selectivity of excitatory neurons were significantly higher than the inhibitory neurons (area, p = 0.0314; half-width, p = 0.0035; Mann–Whitney U test).

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Discussion

Methods

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