Phase sensitivities, excitatory summation fields, and silent suppressive receptive fields of single neurons in the parastriate cortex of the cat

Abstract

Romo PA, Wang C, Zeater N, Solomon SG, Dreher B. Phase sensitivities, excitatory summation fields, and silent suppressive receptive fields of single neurons in the parastriate cortex of the cat. J Neurophysiol 106: 1688 -1712, 2011. First published June 29, 2011 doi:10.1152/jn.00894.2010We have recorded single-neuron activity from cytoarchitectonic area 18 of anesthetized (0.4 -0.7% isoflurane in 65% N 2 O-35% O 2 gaseous mixture) domestic cats. Neurons were identified as simple or complex on the basis of the ratios between the phase-variant (F1) component and the mean firing rate (F0) of spike responses to optimized (orientation, direction, spatial and temporal frequencies, size) high-contrast, luminance-modulated, sinewave drifting gratings (simple: F1/F0 spike-response ratios Ͼ 1; complex: F1/F0 spike-response ratios Ͻ 1). The predominance (ϳ80%) of simple cells among the neurons recorded from the principal thalamorecipient layers supports the idea that most simple cells in area 18 might constitute a putative early stage in the visual information processing. Apart from the "spike-generating" regions (the classical receptive fields, CRFs), the receptive fields of threequarters of area 18 neurons contain silent, extraclassical suppressive regions (ECRFs). The spatial extent of summation areas of excitatory responses was negatively correlated with the strength of the ECRFinduced suppression of spike responses. Lowering the stimulus contrast resulted in an expansion of the summation areas of excitatory responses accompanied by a reduction in the strength of the ECRFinduced suppression. The spatial and temporal frequency and orientation tunings of the ECRFs were much broader than those of the CRFs. Hence, the ECRFs of area 18 neurons appear to be largely "inherited" from their dorsal thalamic inputs. In most area 18 cells, costimulation of CRFs and ECRFs resulted in significant increases in F1/F0 spike-response ratios, and thus there was a contextually modulated functional continuum between the simple and complex cells. luminance-modulated gratings; simple and complex cells; spatial and temporal properties; classical and extraclassical receptive fields; primary visual cortex HUBEL AND WIESEL (1965) postulated that in the domestic cat, the so-called parastriate cortex (cytoarchitectonic area 18 of Gurewitsch and Chatschaturian 1928; cf. Otsuka and Hässler 1962) constitutes a "higher order" visual cortical area (Fig.

Binocular Neurons in Parastriate Cortex: Interocular ‘Matching’ of Receptive Field Properties, Eye Dominance and Strength of Silent Suppression

“…Consistent with our recent study of area 18 [29], in a proportion of cells further increases of the grating size resulted in substantial reduction of magnitude of response or even complete abolishment (suppression) of the response. In some cells however, further increases of the grating size resulted in no change in the magnitude of response (response saturation).…”

“…Summation receptive fields (sRF) are defined here as the regions stimulation of which with optimized (optimal orientation, direction, spatial and temporal frequencies) high-contrast (≥80%) grating patches result in the maximal spike discharge rate [29]. In most cells, the stimulation of region surrounding the sRF (without encroaching on sRF) did not produce action potentials (spikes) but was found to modulate the magnitude of spike-response of the cell when stimulated in conjunction with its sRF.…”

“…This region is defined as the silent extra-classical receptive field (ECRF). The sRF diameters of neurons in cat's area 18 are usually ∼ three-fold greater than those of their minimum discharge fields and thus include not only the discharge fields but also part of the silent receptive field [29]. For each binocular neuron, the properties of both the sRF and the ECRF were assessed monocularly by presenting the stimuli through one eye while the other eye was covered with an occluder not transparent to light.…”

“…Our confidence is based on the location of the discharge field within 5–10° from representation of the vertical meridian and typical area 18 receptive field properties [29], [47]. Furthermore, on occasions when we have made more medial penetrations closer to presumed area 17, the receptive fields of neurons encountered in these penetrations moved close to the representation of the vertical meridian the discharge fields became smaller and preferred higher spatial frequencies [28], [29], [48]. Finally, the areal location (area 18 vs. area 17) of recorded neurons was asessed histologically.…”

“…Parastriate cortex (cytoarchitectonic area 18) of carnivores such as domestic cat, constitutes a distinct part of primary visual cortex, which like the striate cortex receives its principal direct dorsal thalamic input from the LGNd [27]–[29]. As in the case of area 17, the eye-specfic LGNd inputs to area 18 are spatially segregated and there are clear eye dominance columns in this area [9], [10], [30]–[34].…”