Auditory cortex shapes sound responses in the inferior colliculus

Elife. 2020 Jan 31;9:e51890. doi: 10.7554/eLife.51890.

Abstract

The extensive feedback from the auditory cortex (AC) to the inferior colliculus (IC) supports critical aspects of auditory behavior but has not been extensively characterized. Previous studies demonstrated that activity in IC is altered by focal electrical stimulation and pharmacological inactivation of AC, but these methods lack the ability to selectively manipulate projection neurons. We measured the effects of selective optogenetic modulation of cortico-collicular feedback projections on IC sound responses in mice. Activation of feedback increased spontaneous activity and decreased stimulus selectivity in IC, whereas suppression had no effect. To further understand how microcircuits in AC may control collicular activity, we optogenetically modulated the activity of different cortical neuronal subtypes, specifically parvalbumin-positive (PV) and somatostatin-positive (SST) inhibitory interneurons. We found that modulating the activity of either type of interneuron did not affect IC sound-evoked activity. Combined, our results identify that activation of excitatory projections, but not inhibition-driven changes in cortical activity, affects collicular sound responses.

Keywords: auditory cortex; auditory processing; electrophysiology; inferior colliculus; mouse; neuroscience; optogenetics.

Plain Language Summary

How do we hear the world around us? Hearing begins when hair cells in the inner ear translate incoming sound waves into electrical signals. These signals travel via the auditory nerve and the brainstem to the midbrain, where an area called the inferior colliculus processes them. The inferior colliculus then passes the signals on to another area deep within the brain, the thalamus, which processes the signals further before it too passes them on to an area of the brain’s outer layer called the auditory cortex. At each stage of the auditory pathway, the signals undergo more complex processing than at the previous stage. Researchers have tended to think of this pathway as a one-way route from the ear to the brain. But in reality, feedback occurs at various points along the pathway, enabling areas that do higher processing to shape the responses of areas earlier in the pathway. This feedback is particularly prevalent in the auditory system, where one such strong feedback route is from the auditory cortex to the inferior colliculus. This reverse connection helps animals learn new behavioral responses to sounds, for example, to run away from a loud noise. By manipulating the activity of this pathway in mice using a technique called optogenetics, Blackwell et al. provide further clues to how the auditory pathway works. Optogenetics involves introducing light-sensitive ion channels into neurons, and then using light to activate or inhibit those neurons on demand. Blackwell et al. show that activating the feedback pathway from the auditory cortex to the inferior colliculus in awake mice changes how the inferior colliculus responds to sounds. By contrast, inhibiting the pathway has no effect on inferior colliculus responses. This suggests that the feedback pathway is not active all the time, but instead influences inferior colliculus activity only during specific behavior, for example, perhaps when we are listening for a specific sound like the ringing of a phone. Understanding how the brain processes sound is important for understanding how we communicate and why we appreciate music. It could also help in treating hearing loss. Stimulating the inferior colliculus using a device implanted in the brainstem can improve hearing in people with certain types of deafness. Strengthening or weakening the feedback pathway from the auditory cortex to the inferior colliculus could make these implants more effective. In the future, it may even be possible that stimulating the pathway directly could restore hearing without any implant being required.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation
  • Animals
  • Auditory Cortex / physiology*
  • Feedback, Sensory / physiology
  • Female
  • Inferior Colliculi / physiology*
  • Interneurons / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Optogenetics

Associated data

  • Dryad/10.5061/dryad.1t61c80