• We trained adult rats to detect a 5 kHz target tone to receive a food reward. • Training altered target-evoked CSD profiles at the 10 kHz site in A1. • Target-evoked responses were enhanced in layer 2/3 but not layer 4. • Each rat's performance correlated with amplitude of target-evoked current sink. • We conclude that plasticity along intracortical pathways is important for auditory learning.
Auditory-cued behavioral training can alter neural circuits in primary auditory cortex (A1), but the mechanisms and consequences of experience-dependent cortical plasticity are not fully understood. To address this issue, we trained adult rats to detect a 5 kHz target in order to receive a food reward. After 14 days training we identified three locations within A1: (i) the region representing the characteristic frequency (CF) 5 kHz, (ii) a nearby region with CF ˜10 kHz, and (iii) a more distant region with CF ˜20 kHz. In order to compare functional connectivity in A1 near to, vs. far from, the representation of the target frequency, we placed a 16-channel multiprobe in middle- (˜10 kHz) and high- (˜20 kHz) CF regions and obtained current-source density (CSD) profiles evoked by a range of tone stimuli (CF ± 1–3 octaves in quarter-octave steps). Our aim was to construct “CSD receptive fields” (CSD RFs) in order to determine the laminar and spectral profile of tone-evoked current sinks, and infer changes to thalamocortical and intracortical inputs. Behavioral training altered CSD RFs at the 10 kHz, but not 20 kHz, site relative to CSD RFs in untrained control animals. At the 10 kHz site, current sinks evoked by the target frequency were enhanced in layer 2/3, but the initial current sink in layer 4 was not altered. The results imply training-induced plasticity along intracortical pathways connecting the target representation with nearby cortical regions. Finally, we related behavioral performance (sensitivity index, d′) to CSD responses in individual animals, and found a significant correlation between the development of d′ over training and the amplitude of the target-evoked current sink in layer 2/3. The results suggest that plasticity along intracortical pathways is important for auditory learning.