Orientation Selectivity And Spatial Summation Sub-compartments Within The Pinwheel-like-orientation Column In Cat Primary Visual Cortex

Selectivity for the orientation of a visual stimulus is an emergent property of neurons in the primary visual cortex. Neurons sharing a similar orientation preference are arranged in an orientation column with a radial. The mechanisms of orientation selectivity are still debated. The relationship between orientation column and spatial summation clusters, however, remains unclear.In the present study, we tested the orientation tuning property of the classical receptive field(CRF) by extracellular recordings from 168 neurons in cat V1. There is a wide diversity of orientation selectivity(bandwidth and circular variance, CV) in primary visual cortex. We observed that there was a strong correlation between tuning width and aspect ratio of the CRF, a weak correlation between CV and aspect ratio. We demonstrated that circular variance and orthogonal-to-preferred response ratio(O/P ratio), a moderate correlation between tuning width and O/P ratio. Moreover, we demonstrated that suppression far from the peak that could account for the lower circular variance in cat V1 cells may also contribute to narrowing the tuning width of cells. We also studied the dependence of orientation selectivity on the modulation ratio for each cell, which was consistent with robust entrainment of the neural response to the phase of the drifting grating stimulus. We found that there were significant correlations of circular variance and tuning width, with the modulation ratio.Based on the presence or absence of surround suppression, measured by the suppression index at the optimal orientation of the cells, we subdivided the neurons into two categories: surround-suppressive(SS) cells and surround-non-suppressive(SN) cells. When stimulated with an optimally oriented grating centered at CRF, the SS cells showed increasing surround suppression when the stimulus grating was expanded beyond the boundary of the CRF, whereas for the SN cells, expanding the stimulus grating beyond the CRF caused no suppression of the center response. For the SS cells, strength of surround suppression was dependent on the relative orientation between CRF and nCRF: an iso-orientation grating over center and surround at the optimal orientation evoked strongest suppression and a surround grating orthogonal to the optimal center grating evoked the weakest or no suppression. By contrast, the SN cells showed slightly increased responses to an iso-orientation stimulus and weak suppression to orthogonal surround gratings. This iso-/orthogonal orientation selectivity between center and surround was analyzed in 22 SN and 97 SS cells, and for the two types of cells, the different center-surround orientation selectivity was dependent on the suppressive strength of the cells.To reveal the relationship between suppression strength and spatial frequency tuning property, we subdivided 201 V1 neurons into two distinct categories: surround-suppressive(SS) cells and surround-no-suppressive(SN) cells. Consistent with previous reports, we have found that there is a negative correlation between the size of CRF and the optimal spatial frequency(SF) of circular patches of achromatic gratings presented in cells’ receptive fields. Furthermore, we have found a positive correlation between the strength of surround suppression and optimal spatial frequency of achromatic gratings presented in cells’ receptive fields. The correlation between the strength of surround suppression and optimal spatial frequency was stronger in neurons with suppressive regions located in the so-called ’end’ zones.The relationship between iso-orientation domains(IOD) around pinwheel centers(PC) remains unclear. Combining optical imaging, local field potential(LFP) and single-unit recordings, we showed that the pinwheel-like-orientation columns could be subdivided into three sub-compartments based on spatial summation properties of the neurons. The first group showed strong orientation-independent surround suppression, clustered around the PC. The second group revealed strong orientation-dependent surround suppression, located in the median of an IOD. The third group was positioned in the periphery of an IOD, showing weak or no suppression in the surround.We found that:(1) there was a strong correlation between circular variance(CV) and orthogonal-to-preferred response ratio(O/P ratio), and a moderate correlation between tuning width and O/P ratio, moreover, the suppression far from the peak that accounted for the lower CV in cat V1 cells also contributed to the narrowing of the tuning width of cells.(2) SN cells are suitable to detect orientation continuity or similarity between CRF and nCRF, whereas the SS cells are adapted to the detection of discontinuity or differences in orientation between CRF and nCRF.(3) we found a positive correlation between the strength of the surround suppression and the optimal spatial frequency of the achromatic gratings presented in the cells’ receptive fields. The correlation between the strength of surround suppression and the optimal spatial frequency was stronger in neurons with suppressive regions located in the so-called ‘end’ zones.(4) we observed that within the orientation-pinwheel-like structure, three concentric sub-regions could be further subdivided based on the differences in spatial summation property and in size of the receptive fields of the composed neurons. These observations are significant for further understanding the functional modules of the visual cortex and may provide valuable bases of the neural mechanisms for integrating different visual features.