Sensory input directs spatial and temporal plasticity in primary auditory cortex

The cortical representation of the sensory environment is continuously modi fied by experience. Changes in spatial (receptive field) and temporal respo nse properties of cortical neurons underlie many forms of natural learning. The scale and direction of these changes appear to be determined by specif ic features of the behavioral tasks that evoke cortical plasticity. The neu ral mechanisms responsible for this differential plasticity remain unclear partly because important sensory and cognitive parameters differ among thes e tasks. In this report, we demonstrate that differential sensory experienc e directs differential plasticity using a single paradigm that eliminates t he task-specific variables that have confounded direct comparison of previo us studies. Electrical activation of the basal forebrain (BF) was used to g ate cortical plasticity mechanisms. The auditory stimulus paired with BF st imulation was systematically varied to determine how several basic features of the sensory input direct plasticity in primary auditory cortex (A1) of adult rats. The distributed cortical response was reconstructed from a dens e sampling of A1 neurons after 4 wk of BF-sound pairing. We have previously used this method to show that when a tone is paired with BF activation, th e region of the cortical map responding to that tone frequency is specifica lly expanded. In this report, we demonstrate that receptive-field size is d etermined by features of the stimulus paired with BF activation. Specifical ly, receptive fields were narrowed or broadened as a systematic function of both carrier-frequency variability and the temporal modulation rate of pai red acoustic stimuli. For example, the mean bandwidth of A1 neurons was inc reased (+60%) after pairing BF stimulation with a rapid train of tones and decreased (-25%) after pairing unmodulated tones of different frequencies. These effects are consistent with previous reports of receptive-field plast icity evoked by natural learning. The maximum cortical following rate and m inimum response latency were also modified as a function of stimulus modula tion rate and carrier-frequency variability. The cortical response to a rap id train of tones was nearly doubled if BF stimulation was paired with rapi d trains of random carrier frequency, while no following rate plasticity wa s observed if a single carrier frequency was used. Finally, we observed sig nificant increases in response strength and total area of functionally defi ned A1 following BF activation paired with certain classes of stimuli and n ot others. These results indicate that the degree and direction of cortical plasticity of temporal and receptive-field selectivity are specified by th e structure and schedule of inputs that co-occur with basal forebrain activ ation and suggest that the rules of cortical plasticity do not operate on e ach elemental stimulus feature independently of others.