Unraveling the Biology of Auditory Learning: A Cognitive–Sensorimotor–Reward Framework
Trends in Cognitive Sciences
The auditory system is stunning in its capacity for change: a single neuron can modulate its tuning in minutes. Here we articulate a conceptual framework to understand the biology of auditory learning where an animal must engage cognitive, sensorimotor, and reward systems to spark neural remodeling. Central to our framework is a consideration of the auditory system as an integrated whole that interacts with other circuits to guide and refine life in sound. Despite our emphasis on the auditory
... stem, these principles may apply across the nervous system. Understanding neuroplastic changes in both normal and impaired sensory systems guides strategies to improve everyday communication. Learning, Language, and Communication Nervous system plasticity has been observed across the animal kingdom from single cells to sophisticated circuits. Sensory systems are prodigious in their ability to reshape response properties following learning, and in the auditory system plasticity has been observed from cochlea to cortex. This learning is fundamental to our ability to function in and adapt to our environments. Experience navigating this sensory world drives language developmentperhaps the most remarkable auditory learning task humans accomplishand it is necessary to understand the principles that govern this plasticity to devise strategies to improve language and communication in normal and disordered systems. Here we argue that cognitive, sensorimotor, and reward ingredients engender biological changes in sound processing. The mechanisms behind these changes lie in two sets of dichotomous systems: (i) the afferent projections that transmit signals from ear to brain and the efferent projections that propagate signals from brain to ear; and (ii) the primary and nonprimary processing streams that suffuse the auditory neuraxis (Figure 1) . We highlight experiments that advance our understanding of the neurophysiological foundations underlying auditory processing (see Glossary) and that offer objective markers of auditory processing in humans. Finally, we place learning in the context of a distributed, but integrated, auditory system. Rethinking the Auditory System: A Distributed, but Integrated, Circuit Traditional models characterized the auditory system as series of relay stations along an assembly line, each with distinct functions    . While these hierarchical models recognized the interconnectivity of the system, the emphasis was to characterize each nucleus's specialization. The idea was that understanding each station would build each block necessary to construct the auditory circuit, and this 'inside-out' approach has contributed greatly to our understanding of auditory neurophysiology. Trends The auditory system should be thought of as a distributed, but integrated, circuit that is more than a simple set of processing stations. Experiences sculpt the auditory system and impart a biological 'memory' that can change automatic response properties from cochlea to cortex. The cognitive, sensorimotor, and reward aspects of these experiences optimize auditory learning.