Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex

We examined the spatiotemporal organization of ongoing activity in cat visual areas 17 and 18, in relation to the spontaneous activity of individual neurons. To search for coherent activity, voltage-sensitive dye signals were correlated with the activity of single neurons by the use of spike-triggered averaging. In each recording session an area of at least 2 x 2 mm of cortex was imaged, with 124 diodes. In addition, electrical recordings from two isolated units, the local field potential (LFP) from the same microelectrodes, and the surface electroencephalogram (EEG) were recorded simultaneously. 2. The optical signals recorded from the dye were similar to the LFP recorded from the same site. Optical signals recorded from different cortical sites exhibited a different time course. Therefore real-time optical imaging provides information that is equivalent in many ways to multiple-site LFP recordings. 3. The spontaneous firing of single neurons was highly correlated with the optical signals and with the LFP. In 88% of the neurons recorded during spontaneous activity, a significant correlation was found between the occurrence of a spike and the optical signal recorded in a large cortical region surrounding the recording site. This result indicates that spontaneous activity of single neurons is not an independent process but is time locked to the firing or to the synaptic inputs from numerous neurons, all activated in a coherent fashion even without a sensory input. 4. For the cases showing correlation with the optical signal, 27-36% of the optical signal during spike occurrence was directly related to the occurrence of spontaneous spikes in a single neuron, over an area of 2 x 2 mm. In the same cortical area, 43-55% of the activity was directly related to the visual stimulus. 5. Surprisingly, we found that the amplitude of this coherent ongoing activity, recorded optically, was often almost as large as the activity evoked by optimal visual stimulation. The amplitude of the ongoing activity that was directly and reproducibly related to the spontaneous spikes of a single neuron was, on average, as high as 54% of the amplitude of the visually evoked response that was directly related to optimal sensory stimulation, recorded optically. 6. Coherent activity was detected even at distant cortical sites up to 6 mm apart.(ABSTRACT TRUNCATED AT 400 WORDS)