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Role of the striatum in incidental learning of sound categories

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Significance Humans are born as “universal listeners.” However, over the first year, infants’ perception is shaped by native speech categories. How do these categories naturally emerge without explicit training or… Click to show full abstract

Significance Humans are born as “universal listeners.” However, over the first year, infants’ perception is shaped by native speech categories. How do these categories naturally emerge without explicit training or overt feedback? Using fMRI, we examined the neural basis of incidental sound category learning as participants played a videogame in which sound category exemplars had functional utility in guiding videogame success. Even without explicit categorization of the sounds, participants learned functionally relevant sound categories that generalized to novel exemplars when exemplars had an organized distributional structure. Critically, the striatum was engaged and functionally connected to the auditory cortex during game play, and this activity and connectivity predicted the learning outcome. These findings elucidate the neural mechanism by which humans incidentally learn “real-world” categories. Humans are born as “universal listeners” without a bias toward any particular language. However, over the first year of life, infants’ perception is shaped by learning native speech categories. Acoustically different sounds—such as the same word produced by different speakers—come to be treated as functionally equivalent. In natural environments, these categories often emerge incidentally without overt categorization or explicit feedback. However, the neural substrates of category learning have been investigated almost exclusively using overt categorization tasks with explicit feedback about categorization decisions. Here, we examined whether the striatum, previously implicated in category learning, contributes to incidental acquisition of sound categories. In the fMRI scanner, participants played a videogame in which sound category exemplars aligned with game actions and events, allowing sound categories to incidentally support successful game play. An experimental group heard nonspeech sound exemplars drawn from coherent category spaces, whereas a control group heard acoustically similar sounds drawn from a less structured space. Although the groups exhibited similar in-game performance, generalization of sound category learning and activation of the posterior striatum were significantly greater in the experimental than control group. Moreover, the experimental group showed brain–behavior relationships related to the generalization of all categories, while in the control group these relationships were restricted to the categories with structured sound distributions. Together, these results demonstrate that the striatum, through its interactions with the left superior temporal sulcus, contributes to incidental acquisition of sound category representations emerging from naturalistic learning environments.

Keywords: sound category; category learning; sound categories; striatum; group

Journal Title: Proceedings of the National Academy of Sciences of the United States of America
Year Published: 2019

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