Conditioned tone control of brain reward behavior produces highly specific representational gain in the primary auditory cortex

Primary sensory cortices have been assumed to serve as stimulus analyzers while cognitive functions such as learning and memory have been allocated to “higher” cortical areas. However, the primary auditory cortex (A1) is now known to encode the acquired significance of sound as indicated by associatively-induced specific shifts of tuning to the frequencies of conditioned stimuli (CS) and gains in area of CS representations. Rewarding brain stimulation can be a very powerful motivator and brain reward systems have been implicated in addictive behavior. Therefore, it is possible that a cue for brain reward will gain cortical territory and perhaps thereby increase its control of subsequent behavior. To investigate the effect of brain reward on cortical organization, adult male rats (n = 11) were first tested with varying amounts of stimulation of the ventral tegmental area (VTAstm) to generate sigmoidal psychometric functions of nose poke (NP) rates as a function of reward magnitude (duration). Next, we attempted to accomplish tone control of NPs by maintaining intertrial NPs using a low reward duration and presenting a 20 s tone (2.0 kHz, 70 dB) which signaled an increase in reward to a high magnitude 10 s after tone onset. Tone control was demonstrated by a significant increase in the rate of NPs during the first 10 s of tone presentation, which anticipated the delivery of the high magnitude of reward. Tone control was achieved in seven of 11 subjects. This was accompanied by a highly specific and significant gain in representational area, specifically for the half-octave range centered on the CS frequency. However, this plasticity developed only in tone-controlled (TC) animals. The auditory cortex of non-tone-controlled subjects (n = 4) did not differ from that of naïve controls (n = 9) although their VTAstm was as rewarding as for the TC group. These findings reveal that auditory instrumental behavior can be controlled by rewarding VTAstm and that such control appears necessary for the highly specific recruitment of cortical cells to increase the representation of a sound that acquires behavioral importance.