Differential frequency conditioning enhances spectral contrast sensitivity of units in auditory cortex (field Al) of the alert Mongolian gerbil.

Abstract

Differential aversive auditory conditioning in the awake Mongolian gerbil was performed during single- and multi-unit recording in field Al of the primary auditory cortex. Presentations of pure tone stimuli of a given frequency (reinforced conditioned stimulus; CS+) paired with electrocutaneous stimulation (unconditioned stimulus) were combined with several other non-reinforced tone stimuli (non-reinforced conditioned stimulus; CS-). Stimulus presentation during training and testing was optimized for constancy of the probability of occurrence of both the CS+ and the CS- stimulus. The paradigm led to a reorganization of both the spectral and temporal response characteristics of auditory cortical neurons with the following basic results. First, tone-evoked responses of Al neurons recorded after multiple acoustic stimulation under these conditions varied statistically around a mean value (stationarity). Conditioning produced a shift in mean values of evoked responses. The altered tone responses were also stationary (stability of the plastic effects). Second, the frequency-receptive fields (FRFs) of neurons were reorganized in a frequency-specific way such that the CS+ frequency became located in a local minimum of the FRF after training. This resulted from a training-induced increase in the responses to frequencies adjacent to the CS+ frequency in the FRF relative to the CS+ response. The effect can be interpreted as an enhancement of the 'spectral contrast' sensitivity of the unit in the CS+ neighbourhood. Third, apart from this frequency-specific plastic effect, responses to other frequencies also underwent changes during training. The non-frequency-specific changes were not generally predictable but the post-trial responses were stationary. Fourth, the analysis of the long-term behaviour of FRF reorganization revealed the stability of plastic effects under retention training and the gradual re-establishment of the pretrial FRF during extinction training. Fifth, not only the spectral characteristics but also the temporal structure of the tone-evoked responses could be affected by the training. In most cases the training-induced changes measured within the first tens of milliseconds of the response corresponded to the response changes obtained by integration over the total response period. There were some cases, however, in which the direction of the response change varied with time, indicating that excitatory and inhibitory influences on the temporal response pattern were differently affected by training.