Hearing involves analyzing the physical attributes of sounds and integrating the results of this analysis with other sensory, cognitive, and motor variables in order to guide adaptive behavior. The auditory cortex is considered crucial for the integration of acoustic and contextual information and is thought to share the resulting representations with subcortical auditory structures via its vast descending projections. By imaging cellular activity in the corticorecipient shell of the inferior colliculus of mice engaged in a sound detection task, we show that the majority of neurons encode information beyond the physical attributes of the stimulus and that the animals' behavior can be decoded from the activity of those neurons with a high degree of accuracy. Surprisingly, this was also the case in mice in which auditory cortical input to the midbrain had been removed by bilateral cortical lesions. This illustrates that subcortical auditory structures have access to a wealth of non-acoustic information and can, independently of the auditory cortex, carry much richer neural representations than previously thought.
Keywords: auditory; cortex; corticocollicular; feedback; midbrain; mouse; neuroscience; sound detection.
Making sense of a sound and responding to it appropriately requires various parts of the nervous system to work together in a hierarchical and interconnected manner. For example, after the ear converts sound vibrations into electric signals, this information is sent to and pre-processed by the midbrain, a brain structure tasked with linking the auditory brain stem to sensory and motor systems. The signals are then relayed to the auditory cortex where they are further decoded and integrated with information emerging from other sensory and behavioral systems. These integrated auditory signals can then be fed back to the midbrain, potentially adjusting the signals delivered to its downstream targets. Due to its integrative nature, neural activity in the auditory cortex is also shaped by non-acoustic input. Yet a growing body of evidence points to auditory neurons present in other regions than the cortex, such as the midbrain, being able to respond to non-acoustic information as well. It has typically been assumed that such responses are mediated by feedback from the auditory cortex. To test this assumption, Lee et al. recorded the activity of auditory neurons in the midbrain of mice performing a sound detection task (that is, responding to a clicking sound by licking a waterspout). The analyses showed that most cells encoded not only basic sound properties (such as amplitude) but also information about the animal’s behavioral response; in fact, the performance of an animal could be accurately inferred based on the activity patterns of such neurons. This was the case even in mice in which the auditory cortex had been removed, suggesting that the activity detected in the midbrain had not emerged due to cortical signals. The findings by Lee et al. help refine our understanding of the brain processes that underpin hearing, in particular by highlighting tight links between behavioral information and neural activity in the midbrain. These results should help guide further research into how various brain regions participate in the processing of auditory input and the production of sound-guided behaviors, including when these mechanisms are affected by factors such as health or disease.
© 2023, Lee et al.