Multiple non-auditory cortical regions innervate the auditory midbrain

Abstract

Our perceptual experience of sound depends on the integration of multiple sensory and cognitive domains, but the networks sub-serving this integration are unclear. There are connections linking different cortical domains, however we do not know if there are also connections between multiple cortical domains and subcortical structures. Retrograde tracing in rats revealed that the inferior colliculus -the auditory midbrain -receives dense descending projections from not only the auditory cortex, but also the visual, somatosensory, motor, and prefrontal cortices. While all these descending connections are bilateral, those from sensory areas show a more pronounced ipsilateral dominance than those from motor and prefrontal cortices. Anterograde tracing from cortical areas identified by retrograde tracing, showed cortical fibres terminating in all three subdivisions of the inferior colliculus, targeting both inhibitory and excitatory neurons. These findings demonstrate that auditory perception is served by a network that includes extensive descending connections from sensory, behavioural, and executive cortices.

Tonotopic and non-auditory organization of the mouse dorsal inferior colliculus revealed by two-photon imaging

“…These cells seemed to be enriched at the caudolateral side of the dorsal IC (Figure 8C–D). Four of the 41 cells were found in the Gad2;Ai96 line, in agreement with a recent report that inputs from motor or somatosensory cortex can directly target GABAergic cells (Olthof et al, 2019), and the remainder in the GP4.3 line, making them 1% of GABAergic and 4% of investigated glutamatergic cells, respectively.…”

“…Numerous studies have shown both ascending and descending somatosensory projections to the IC (Aitkin et al, 1981; Künzle, 1998; Jain and Shore, 2006; Zhou and Shore, 2006; Lesicko et al, 2016; Patel et al, 2017), as well as from nuclei that are upstream from IC such as the dorsal cochlear nucleus, which also receive somatosensory inputs (Wu et al, 2014). In addition, the IC receives inputs from the motor cortex (Cooper and Young, 1976; Olthof et al, 2019). This prompted us to investigate whether these ‘spontaneous’ activities could be attributed to non-auditory inputs.…”

Descending Axonal Projections from the Inferior Colliculus Target Nearly All Excitatory and Inhibitory Cell Types of the Dorsal Cochlear Nucleus

“…Inputs from IC may convey nonauditory "multisensory" signals and could be one of the main sources of multisensory input to DCN to underlie functions such as cancellation of self-generated sounds. The IC is a major hub of multisensory integration, processing axonal inputs from somatosensory, visual and auditory cortices (Cooper and Young, 1976;Olthof et al, 2019), and somatosensory brainstem nuclei (Tokunaga et al, 1984;Paloff and Usunoff, 1992). The cell types in the granule cell region are known to process extrinsic nonauditory signals from regions of various modalities, and the relative balance among these contributions is unclear (Ryugo et al, 2003).…”