A fundamental step in visual pattern recognition is the establishment of relations between spatially separate features. Recently, we have shown that neurons in the cat visual cortex have oscillatory responses in the range 40-60 Hz (refs 1, 2) which occur in synchrony for cells in a functional column and are tightly correlated with a local oscillatory field potential. This led us to hypothesize that the synchronization of oscillatory responses of spatially distributed, feature selective cells might be a way to establish relations between features in different parts of the visual field. In support of this hypothesis, we demonstrate here that neurons in spatially separate columns can synchronize their oscillatory responses. The synchronization has, on average, no phase difference, depends on the spatial separation and the orientation preference of the cells and is influenced by global stimulus properties.
In areas 17 and 18 of the cat visual cortex the firing probability of neurons, in response to the presentation of optimally aligned light bars within their receptive field, oscillates with a peak frequency near 40 Hz. The neuronal firing pattern is tightly correlated with the phase and amplitude of an oscillatory local field potential recorded through the same electrode. The amplitude of the local field-potential oscillations are maximal in response to stimuli that match the orientation and direction preference of the local cluster of neurons. Single and multiunit recordings from the dorsal lateral geniculate nucleus of the thalamus showed no evidence of oscillations of the neuronal firing probability in the range of 20-70 Hz. The results demonstrate that local neuronal populations in the visual cortex engage in stimulus-specific synchronous oscillations resulting from an intracortical mechanism. The oscillatory responses may provide a general mechanism by which activity patterns in spatially separate regions of the cortex are temporally coordinated.The mechanism by which populations of neurons in the cerebral cortex temporally coordinate their activity patterns in response to specific sensory stimuli constitutes a basic unresolved question in sensory physiology. In the vertebrate olfactory system the spatiotemporal coordination of neuronal activity is achieved by the synchronization of oscillatory responses having a frequency in the range of 40-80 Hz (1-5). Evidence suggesting that a similar mechanism for the synchronization of activity may operate in the neocortex has come from field potential recordings in awake animals. It has been demonstrated that oscillatory activity in the high betafrequency range (20-50 Hz) occurs in sensory areas of the neocortex when the animals direct their attention to meaningful stimuli (6-11).Previously we have discovered, from recordings in area 17 of awake kittens, that neuronal responses recorded during periods of behavioral attention exhibit a rhythmic firing pattern that is tightly correlated with an oscillatory local field potential (LFP) having a frequency near 40 Hz (12). Thus, we sought to determine whether the oscillatory responses could also be recorded under varying conditions of anesthesia that would permit a more quantitative analysis of both their stimulus specificity as well as their temporal properties. Here, we extend our previous observations (13) and report that local groups of neurons, within functional columns ofthe visual cortex, engage in stimulus-specific oscillatory responses having a frequency near 40 Hz. This periodic neuronal activity is tightly correlated to the simultaneously recorded LFP, which in the majority of recordings has a similar orientation and direction preference as the local cluster of neurons. No comparable oscillations of firing probability were found for the thalamic input to visual cortex, indicating that the generation of oscillatory responses is a cortical phenomenon. The results suggest the hypothesis that the temporal pat...
In response to visual stimulation, a subset of neurons in the striate and prestriate cortex displays synchronous rhythmic firing in the gamma frequency band (20 to 70 hertz). This finding has raised two fundamental questions: What is the functional significance of synchronous gamma-band activity and how is it generated? This report addresses the second of these two questions. By means of intracellular recording and staining of single cells in the cat striate cortex in vivo, a biophysically distinct class of pyramidal neuron termed "chattering cells" is described. These neurons are located in the superficial layers of the cortex, intrinsically generate 20- to 70-hertz repetitive burst firing in response to suprathreshold depolarizing current injection, and exhibit pronounced oscillations in membrane potential during visual stimulation that are largely absent during periods of spontaneous activity. These properties suggest that chattering cells may make a substantial intracortical contribution to the generation of synchronous cortical oscillations and thus participate in the recruitment of large populations of cells into synchronously firing assemblies.
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