Functional Heterogeneity in Neighboring Neurons of Cat Primary Visual Cortex in Response to Both Artificial and Natural Stimuli

Neurons in primary visual cortex of many mammals are clustered according to their preference to stimulus parameters such as orientation and spatial frequency. Nevertheless, responses to complex visual stimuli are highly heterogeneous between adjacent neurons. To investigate the relation between these observations, we recorded from pairs of neighboring neurons in area 17 of anesthetized cats in response to stimuli of differing complexity: sinusoidal drifting gratings, binary dense noise, and natural movies. Comparisons of the tuning curves revealed similar orientation and direction preferences for neighboring neurons, but large differences in preferred phase, direction selectivity, and tuning width of spatial frequency. No pair was similar across all tuning properties. The neurons' firing rates averaged across multiple stimulus repetitions (the signal) were also compared. Binned between 10 and 200 ms, the correlation between these signals was close to zero in the median across all pairs for all stimulus classes. Signal correlations agreed poorly with differences in tuning properties, except for receptive field offset and relative modulation (i.e., the strength of phase modulation). Nonetheless, signal correlations for different stimulus classes were well correlated with each other, even for gratings and movies. Conversely, trial-to-trial fluctuations (termed noise) were poorly correlated between neighboring neurons, suggesting low degrees of common input. In response to gratings and visual noise, signal and noise correlations were well correlated with each other, but less so for responses to movies. These findings have relevance for our understanding of the processing of natural stimuli in a functionally heterogeneous cortical network.