Precise Memory is Predicted by Learning-Induced Sensory System Neurophysiological Plasticity

Abstract

Despite identical learning experiences, individuals differ in the memory formed of those experiences. Memory formed with sensory specificity determines its utility for selectively cueing subsequent behavior, even in novel situations. If an individual forms generalized memory, then there is potential for novel sensory cues to interfere with accurate behavioral performance. Here, a rodent model of auditory learning capitalized on individual differences in learning-induced auditory neuroplasticity to identify and characterize neural substrates for sound-specific (vs. general) memory of the training signal's acoustic frequency. Animals with naturally or pharmacologically induced signal-"specific" memory revealed behaviorally, exhibited longlasting signal-specific neurophysiological plasticity in auditory cortical and subcortical evoked responses, while learning-induced changes were not detected in animals with "general" memories. Individual differences validated this brain-behavior relationship, such that the degree of change in neurophysiological responses could be used to determine the precision of memory formation. Main Text:Individual differences are often intentionally minimized by experimental designs in behavioral neuroscience. Consequently, traditional approaches implicitly treat differences between subjects as "noise" to be overcome by large enough sample sizes to accurately describe and compare the underlying distributions of each group. This philosophical choice stymies an opportunity to use variability as a key to understand brain-behavior relationships. Even when group analyses reveal significant effects, they may not identify the full extent of brain-behavior relationships. Variability in learning, memory, and behavior derives from multiple factors 1-8 each with their own neural generators that have distinct effects on function 9-11 . Therefore, a powerful use of within-group variability is to explain magnitude-of-effect in individual behavioral performance by differences in learning-induced neural function. Indeed, a major goal in behavioral neuroscience is to understand brain-behavior relationships enough to gain the ability to manipulate function and drive behavior in a desired direction by promoting neuroplasticity [12][13][14] . However, to harness plasticity mechanisms in a useful way after the form of experience-induced plasticity between groups is identified, its function and magnitude of effect must be determined at the level of the individual.Previous work has identified distinct functions for different forms of auditory system plasticity related to the behavioral relevance of acoustic frequency 6,15-18 including at different time scales [19][20][21] . For example, in the auditory cortex, rapid changes in neural tuning properties correlate with selective attention to sound frequency during active tasks 21,22 , while long-term changes in tuning bandwidth may be related to frequency-specific memory over time 23,24 . Subcortical neurons in the lemniscal auditory nuclei also exhibit changes in tun...