Contributions of excitation and suppression in shaping spatial frequency selectivity of V1 neurons as revealed by binocular measurements

Abstract

Ninomiya T, Sanada TM, Ohzawa I. Contributions of excitation and suppression in shaping spatial frequency selectivity of V1 neurons as revealed by binocular measurements. J Neurophysiol 107: 2220 -2231, 2012. First published January 11, 2012 doi:10.1152/jn.00832.2010Neurons in the early visual cortex are generally highly sensitive to stimuli presented to the two eyes. However, the majority of studies on spatial and temporal aspects of neural responses were based on monocular measurements. To study neurons under more natural, i.e., binocular, conditions, we presented sinusoidal gratings of a variety of spatial frequencies (SF) dichoptically in rapid sequential flashes and analyzed the data using a binocular reverse correlation technique for neurons in cat area 17. The resulting set of data represents a frequencydomain binocular receptive field from which detailed selectivities, both monocular and binocular, could be obtained. Consistent with previous studies, the responses could generally be explained by linear summation of inputs from the two eyes. Suppressive responses were also observed and were delayed typically by 5-15 ms relative to excitatory responses. However, we have found more diverse nature of suppressive responses than those reported previously. The optimal suppressive frequency could be either higher or lower than that of the excitatory responses. The bandwidth of SF tuning of the suppressive responses was usually broader than that of the excitatory responses. Cells with lower optimal SFs for suppression tended to show high optimal SFs and sharp tuning curves. The dynamic shift of optimal SF from low to high SF was accompanied by suppression with earlier onset and higher peak SF or later onset and lower peak SF than excitation. These results suggest that the suppression plays an essential role in generating the temporal dynamics of SF selectivity.frequency-domain binocular receptive field; cat area 17; reverse correlation VISUAL INFORMATION IS SEPARATELY acquired from two retinae and is first integrated in the early visual cortex. Since Wiesel (1959, 1962) showed that many of the neurons in the early visual cortex could be activated by inputs from either eye, the nature of binocular information processing has been one of the major interests in this stage (Anzai et al. 1999a,b; Bishop et al. 1971;Cumming and DeAngelis 2001; Ohzawa and Freeman 1986a,b;Ohzawa et al. 1990Ohzawa et al. , 1996Ohzawa et al. , 1997Pettigrew et al. 1968).Previous studies performing binocular measurement have mainly been focused on its characteristics in the space domain because the response properties of neurons in the early visual cortex are generally well-described in this domain. However, neurons in this stage exhibit high selectivity for the spatial frequency (SF;Campbell et al. 1969;De Valois et al. 1982;Maffei and Fiorentini 1973), and therefore the SF domain is also useful for capturing the feature of their responses. Many previous studies have revealed the properties of monocular responses in the SF domain Jones...

Organization and Origin of Spatial Frequency Maps in Cat Visual Cortex

“…Instead, these locations could be selective to more complex features and thus not well described by the two distinct parameters representing preferred orientation and preferred SF. This idea is supported by a recent two-photon imaging studies showing a large percentage of unresponsive cells to oriented, drifting gratings close to pinwheels (Ohki et al, 2006). This interpretation recalls the suggestion of Basole et al (2003) that separable cortical maps representing preferred orientation and preferred SF (as well as speed) were not sufficient to predict the preferred orientations within a complex stimulus composed of drifting, oriented textures.…”

“…Finally, the location of the functional "border" between A17 and A18 was estimated based on the difference between the maximal intensity maps at 0.15 and 0.5 cpd (Bonhoeffer et al, 1995;Ohki et al, 2000). The TZ was defined with precision on the basis of the data obtained through GC activation in Figure 11G.…”

“…The signal at pinwheel was assumed to be weak. Indeed, a recent twophoton imaging study has shown that neurons located close to pinwheel centers have a weak response strength and that a large proportion of cells are unresponsive to an oriented, drifting grating (Ohki et al, 2006). For simplicity here, the signal at the pinwheel center was assumed to be of equal strength for the two curves.…”

“…Figures 6A and 10A show that the SF representation in the TZ exhibits local extrema that reflect the patchy organization present in both A17 and A18. The SF representation in the TZ is additionally constrained by the very different ranges of SFs that activate the respective areas, implying the existence of yet another SF gradient to ensure the continuity between the two areas (Bonhoeffer et al, 1995;Issa et al, 2000;Ohki et al, 2000). But previous approaches did not permit this gradient to be precisely characterized.…”

Disparity processing in primary visual cortex

“…If this suppression occurred monocularly, in a cell where there was an excitatory binocular interaction, it would be compatible with the data of both studies above. When a binocular stimulus is presented, raising responses above baseline, suppressive effects of adding a single frequency to one eye are often seen [36]. It is therefore possible that over the range of stimuli explored in all these studies, the two descriptions are functionally equivalent.…”