Complex and spatially segregated auditory inputs of the mouse superior colliculus

Sep 13, 2018The Journal of physiology

Distinct and separate hearing inputs to the mouse movement control area

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Abstract

Three distinct types of neurons were identified in the auditory-recipient layer of the (SC) in mice.

Auditory circuits in the SC deep layers were characterized, revealing intrinsic properties of neurons that correspond to three electrophysiological clusters.
A novel direct excitatory connection was found that drives feed-forward inhibition within the SC.
100% of recorded neurons exhibited a long-range monosynaptic inhibition, despite only about 15% of -projecting neurons being inhibitory.
Distinct spatial patterns were observed in cell body locations and axon trajectories for excitatory and inhibitory inputs.
These findings suggest that sensory integration in the SC is more complex than previously understood.

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KEY POINTS: Although the visual circuits in the (SC) have been thoroughly examined, the auditory circuits lack equivalent scrutiny. SC neurons receiving auditory inputs in mice were characterized and three distinguishable types of neurons were found. The auditory pathways from external nuclei of the inferior colliculus (IC) were characterized, and a novel direct inhibitory connection and an excitation that drives feed-forward inhibitory circuits within the SC were found. The direct excitatory and inhibitory inputs exhibited distinct arbourization patterns in the SC. These findings suggest functional differences between excitatory and inhibitory sensory information that targets the auditory SC.

ABSTRACT: The superior colliculus (SC) is a midbrain structure that integrates auditory, somatosensory and visual inputs to drive orientation movements. While much is known about how visual information is processed in the superficial layers of the SC, little is known about the SC circuits in the deep layers that process auditory inputs. We therefore characterized intrinsic neuronal properties in the auditory-recipient layer of the SC (; SGP) and confirmed three electrophysiologically defined clusters of neurons, consistent with literature from other SC layers. To determine the types of inputs to the SGP, we expressed Channelrhodopsin-2 in the nucleus of the brachium of the inferior colliculus (nBIC) and external cortex of the inferior colliculus (ECIC) and optically stimulated these pathways while recording from SGP neurons. Probing the connections in this manner, we described a monosynaptic excitation that additionally drives feed-forward inhibition via circuits intrinsic to the SC. Moreover, we found a profound long-range monosynaptic inhibition in 100% of recorded SGP neurons, a surprising finding considering that only about 15% of SGP-projecting neurons in the nBIC/ECIC are inhibitory. Furthermore, we found spatial differences in the cell body locations as well as axon trajectories between the monosynaptic excitatory and inhibitory inputs, suggesting that these inputs may be functionally distinct. Taking this together with recent anatomical evidence suggesting an auditory excitation from the nBIC and a GABAergic multimodal inhibition from the ECIC, we propose that sensory integration in the SGP is more multifaceted than previously thought.

Key numbers

100%

Direct Inhibition Presence

Percentage of recorded neurons with direct inhibitory connections.

15%

Inhibitory Neuron Percentage

Percentage of -projecting neurons in the nBIC/ECIC that are inhibitory.

Neuron Types Identified

Number of distinct neuron types found in the layer.

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Complex and spatially segregated auditory inputs of the mouse superior colliculus

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