Primary visual coding can be characterized by the receptive field (RF) properties of single neurons. Subject of this paper is our search for a global, second coding step beyond the RF-concept that links related features in a visual scene. In recent models of visual coding, oscillatory activities have been proposed to constitute such linking signals. We tested the neurophysiological relevance of this hypothesis for the visual system. Single and multiple spikes as well as local field potentials were recorded simultaneously from several locations in the primary visual cortex (A17 and A18) using 7 or 19 individually advanceable fiber-microelectrodes (250 or 330 microns apart). Stimulus-evoked (SE)-resonances of 35-85 Hz were found in these three types of signals throughout the visual cortex when the primary coding channels were activated by their specific stimuli. Stimulus position, orientation, movement direction and velocity, ocularity and stationary flicker caused specific SE-resonances. Coherent SE-resonances were found at distant cortical positions when at least one of the primary coding properties was similar. Coherence was found 1) within a vertical cortex column, 2) between neighbouring hypercolumns, and 3) between two different cortical areas. We assume that the coherence of SE-resonances is mediated by recurrent excitatory intra- and inter-areal connections via phase locking between assemblies that represent the linking features of the actual visual scene. Visually related activities are, thus, transiently labelled by a temporal code that signalizes their momentary association.

^Latencies to small flashing spots of light were measured in different layers of areas V1 and V2 in anesthetized and paralyzed macaque monkeys. The shortest latencies were found in layers 4C alpha and 4B of area V1. Latencies in layer 4C beta were on average 20 ms longer than those in 4C alpha and 4B. The shortest latencies in area V2 were observed in the infragranular layers and they did not differ significantly from those found in the infragranular layers in V1. Similarly, latencies in the supragranular layers of V2 were not significantly different from those measured in the supragranular layers of V1. These results show that, in area V1, neurons of the magnocellular pathway are activated on average 20 ms earlier than those of the parvocellular pathway. Our data also suggest that much processing begins simultaneously in areas V1 and V2

1. Single-unit and multiunit activities were recorded at the area 17-18 border of each cortical hemisphere in paralyzed cats anesthetized with nitrous oxide supplemented with halothane. Cross-correlation histograms (CCHs) were computed between 86 pairs of single units and 99 pairs of multiunit activities. Visually evoked peaks in the CCHs were removed by subtracting the shift predictor. 2. Three types of CCH peaks were observed: T peaks with narrow widths (4-28 ms), C peaks with intermediate widths (30-100 ms), and H peaks with large widths (100-1,000 ms). Oscillatory coupling was observed rarely. This tripartite distribution of CCH peaks is similar to that reported in an earlier study on the temporal coupling between areas 17 and 18. Different types of peaks occurred in isolation or in combination. Combination of different peak types was more often observed in multiunit recordings. 3. CCH peaks of all types were usually centered, meaning that units in opposite hemispheres tend to synchronize their discharges. 4. T peaks were observed almost exclusively for units with overlapping receptive fields and preferentially for units with similar optimal orientations. No dependence on receptive field position or optimal orientation was observed for the encounter rate of C and H peaks. 5. A new method, called the peristimulus CCH, was developed to study the time course of the temporal coupling. This showed that H peaks can occur during visual stimulation and that their time course follows that of the visual responses of the coupled neurons. 6. Using one single bar or two simultaneously presented light bars as stimuli, we studied the effect of visual stimulation on the strength of H coupling. This showed that H coupling observed under stimulation with a single moving light bar can be completely abolished, with little change in visual responses, when the stimulus is changed to two noncoherently moving bars. This was related to a strong decrease of the H peaks in the autocorrelograms. 7. These results demonstrate that T, C, and H peaks constitute, together with high-frequency oscillations, universal forms of temporal coupling between neurons located in different cortical areas. The following paper reports on the effects of cortical lesions on the encounter rate and strength of these different types of coupling.

Visual cortical areas are richly but selectively connected by “patchy” projections. We characterized these connections physiologically with cross-correlograms (CCHs), calculated for neuron pairs or small groups located one each in visual areas 17 and 18 of the cat. The CCHs were then compared to the visuotopic and orientation match of the neurons' receptive fields (RFs).For both spontaneous and visually driven activity, most non-flat correlograms were centered; i.e. the most likely temporal relationship between spikes in the two areas is a synchronous one. Although spikes are most likely to occur simultaneously, area 17 spikes may occur before area 18 or vice versa, giving the cross-correlogram peak a finite width (temporal dispersion). Cross-correlograms fell into one of three groups according to their full-width at half peak height: 1–8 ms (modal width, 3 ms), 15–65 ms (modal width 30 ms), or 100–1000 ms (modal width 400 ms). These classificatory groups are nonoverlapping; the three types of coupling appeared singly and in combination.Neurons whose receptive fields (RFs) are nonoverlapping or cross-oriented may yet be coupled, but the coupling is more likely to be the broadest type of coupling than the medium-dispersed type. The sharpest type of coupling is found exclusively between neurons with at least partially overlapping RFs and mostly between neurons whose stimulus orientation preferences matched to within 22.5 deg. The maximum spatial dispersion observed in the RFs of coupled neurons compares well with the maximum divergence seen anatomically in the A18/A17 projection system.We suggest three different mechanisms to produce each of the three different degrees of observed spatial and temporal coherence. All mechanisms use common input of cortical origin. For medium and broad coupling, this common input arises from cell assemblies split between both sides of the 17/18 projection system, but acting synchronously. Such distributed common-input cell assemblies are a means of overcoming sparse connectivity and achieving synaptic transmission in the pyramidal network.