Auditory space representation and its plasticity in the shell of the inferior colliculus

• Applicant: Dr. Meike Marie Rogalla
• Subject Area: Cognitive, Systems and Behavioural Neurobiology ; Experimental and Theoretical Network Neuroscience
• Term: from 2022 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 509509296

• Final Report Year: 2024

Final Report Abstract

Navigating complex auditory environments requires the brain to effectively encode auditory space. For optimal flexibility, the coding of auditory space must adapt to peripheral changes, such as the loss of binaural information due to monaural hearing loss. Acute monaural hearing loss typically broadens receptive fields and degrades spatial selectivity, affecting sound localization. Remarkably, humans and animals with monaural occlusion can regain sound localization sensitivity, which seems to depend on active participation in localization tasks. This indicates that there must be a plasticity mechanism that enables adaptation of auditory space representation. The dorsal shell of the inferior colliculus (IC) appears to be a dominant site for this learning-induced spatial plasticity. When descending input from the primary auditory cortex to the dorsal shell IC is silenced, animals cannot re-learn sound localization after monaural hearing loss, highlighting the IC shell’s importance in spatial plasticity. Despite this evidence, there is limited understanding of how flexible shell IC neuronal populations are encoding auditory space or how well these population codes can adjust to changes in sensory input. This project explored the adaptability of population coding for auditory space in the dorsal shell IC and examined the effects of monaural hearing loss on this representation, both during passive listening, and active sensing. Using 2-photon Ca2+ imaging in awake, head-fixed mice, we mapped the spatial receptive fields of shell IC neurons under normal binaural conditions and following acute monaural ipsilateral ear plugging. Our results from passively listening mice show that the dorsal shell IC maintains a broad representation of auditory space through dynamic remapping of neuronal responses, instead of the previously proposed reshaping of receptive fields. Furthermore, the activity of some dorsal shell IC neurons of mice performing in a sound localization task showed signs of plasticity mechanisms linked to correct responses on the plugged side. To our knowledge, this is the first project that investigated population responses of the identical neurons across conditions of normal and altered binaural hearing. Our results further established the role of the dorsal shell IC during spatial hearing and deepened our understanding about the physiology of sensory plasticity in adulthood. Furthermore, they established the dorsal shell IC as a unique stage that significantly differs in binaural processing from the central IC and other auditory areas.

Publications

• Talk: “Representation of Auditory Space in the Shell of the Inferior Colliculus” at the Advances and Perspectives in Auditory Neuroscience Meeting (APAN), San Diego, California, USA
  Rogalla, Meike Marie
  
• Auditory Corticofugal Neurons Transmit Auditory and Non-auditory Information During Behavior. The Journal of Neuroscience, 44(7), e1190232023.
  Ford, Alexander N.; Czarny, Jordyn E.; Rogalla, Meike M.; Quass, Gunnar L. & Apostolides, Pierre F.
  
• Differential optogenetic activation of the auditory midbrain in freely moving behaving mice. Frontiers in Systems Neuroscience, 17.
  Rogalla, Meike M.; Seibert, Adina; Sleeboom, Jana M. & Hildebrandt, K. Jannis
  
• Recurrent Circuits Amplify Corticofugal Signals and Drive Feedforward Inhibition in the Inferior Colliculus. The Journal of Neuroscience, 43(31), 5642-5655.
  Oberle, Hannah M.; Ford, Alexander N.; Czarny, Jordyn E.; Rogalla, Meike M. & Apostolides, Pierre F.
  
• Talk : “Representation of Auditory Space in the Shell of the Inferior Colliculus”. The 46th Midwinter Meeting of the Association for Research in Otolaryngology (ARO), Orlando, Florida, USA
  Rogalla, Meike Marie
  
• Mixed Representations of Sound and Action in the Auditory Midbrain. The Journal of Neuroscience, 44(30), e1831232024.
  Quass, Gunnar L.; Rogalla, Meike M.; Ford, Alexander N. & Apostolides, Pierre F.
  
• Population coding of time-varying sounds in the nonlemniscal inferior colliculus. Journal of Neurophysiology, 131(5), 842-864.
  Shi, Kaiwen; Quass, Gunnar L.; Rogalla, Meike M.; Ford, Alexander N.; Czarny, Jordyn E. & Apostolides, Pierre F.
  
• Poster : “Investigating sound localization in head-fixed mice using two-alternative forced choice behavior”. The 47th Midwinter Meeting of the Association for Research in Otolaryngology (ARO), Anaheim, California, USA
  Rogalla, Meike Marie