Organization of response areas in ferret primary auditory cortex.

1. We studied the topographic organization of the response areas obtained from single- and multiunit recordings along the isofrequency planes of the primary auditory cortex in the barbiturate-anesthetized ferret. 2. Using a two-tone stimulus, we determined the excitatory and inhibitory portions of the response areas and then parameterized them in terms of an asymmetry index. The index measures the balance of excitatory and inhibitory influences around the best frequency (BF). 3. The sensitivity of responses to the direction of a frequency-modulated (FM) tone was tested and found to correlate strongly with the asymmetry index of the response areas. Specifically, cells with strong inhibition from frequencies above the BF preferred upward sweeps, and those from frequencies below the BF preferred downward sweeps. 4. Responses to spectrally shaped noise were also consistent with the asymmetry of the response areas. For instance, cells that were strongly inhibited by frequencies higher than the BF responded best to stimuli that contained least spectral energy above the BF, i.e., stimuli with the opposite asymmetry. 5. Columnar organization of the response area types was demonstrated in 66 single units from 16 penetrations. Consistent with this finding, it was also shown that response area asymmetry measured from recordings of a cluster of cells corresponded closely with those measured from its single-unit constituents. Thus, in a local region, most cells exhibited similar response area types and other response features, e.g., FM directional sensitivity. 6. The distribution of the asymmetry index values along the isofrequency planes revealed systematic changes in the symmetry of the response areas. At the center, response areas with narrow and symmetric inhibitory sidebands predominated. These gave way to asymmetric inhibition, with high-frequency inhibition (relative to the BF) becoming more effective caudally and low-frequency inhibition more effective rostrally. These response types tended to cluster along repeated bands that paralleled the tonotopic axis. 7. Response features that correlated with the response area types were also mapped along the isofrequency planes. Thus, in four animals, a map of FM directional sensitivity was shown to be superimposed on the response area map. Similarly, it was demonstrated in six animals that the spectral gradient of the most effective noise stimulus varied systematically along the isofrequency planes. 8. One functional implication of the response area organization is that cortical responses encode the locally averaged gradient of the acoustic spectrum by their differential distribution along the isofrequency planes. This enhances the representation of such features as the symmetry of spectral peaks and edges and the spectral envelope.(ABSTRACT TRUNCATED AT 400 WORDS)