Diversity, heterogeneity and orientation-dependent variation of spike count correlation in the cat visual cortex

Cortical neurons are known to be noisy encoders of information, showing large response variabilities with repeated presentations of identical stimuli. These spike count variabilities are correlated over the cell population and their neuronal mechanism and functional significance have not been well understood. Recently there has been much debate over the magnitude of the population mean of the correlation, ranging from 0.1 to 0.2 down to nearly zero. We performed multi-neuron recordings on the cat visual cortex and found that the population mean did not necessarily represent the nature of correlated variabilities because the spike count correlation showed significant diversity and heterogeneity. Although the population mean was relatively small (0.06), the correlations of individual unit pairs were distributed over a broad range, extending to both positive and negative values. In most of the recording sessions of local cell populations (83%), significantly positive correlations coexisted with significantly negative ones in different unit pairs. Furthermore, nearly 20% of the unit pairs showed significant variation in the spike count correlation for different stimulus orientations. Correlation analysis between the spike count correlation and the firing activity of the unit pair suggested that the orientation tuning properties of the two quantities were unlikely to have originated from a common neuronal mechanism. Diversity, heterogeneity and context-dependent variation suggests that the correlated spike count variabilities originate not from fixed anatomical connections but rather from the dynamic interaction of neuronal networks.