When inspecting visual scenes, primates perform on average four saccadic eye movements per second, which implies that scene segmentation, feature binding, and identification of image components is accomplished in <200 ms. Thus individual neurons can contribute only a small number of discharges for these complex computations, suggesting that information is encoded not only in the discharge rate but also in the timing of action potentials. While monkeys inspected natural scenes we registered, with multielectrodes from primary visual cortex, the discharges of simultaneously recorded neurons. Relating these signals to eye movements revealed that discharge rates peaked around 90 ms after fixation onset and then decreased to near baseline levels within 200 ms. Unitary event analysis revealed that preceding this increase in firing there was an episode of enhanced response synchronization during which discharges of spatially distributed cells coincided within 5-ms windows significantly more often than predicted by the discharge rates. This episode started 30 ms after fixation onset and ended by the time discharge rates had reached their maximum. When the animals scanned a blank screen a small change in firing rate, but no excess synchronization, was observed. The short latency of the stimulation-related synchronization phenomena suggests a fast-acting mechanism for the coordination of spike timing that may contribute to the basic operations of scene segmentation.

The architectonic subdivisions of the brain are believed to be functional modules, each processing parts of global functions. Previously, we showed that neurons in different regions operate in different firing regimes in monkeys. It is possible that firing regimes reflect differences in underlying information processing, and consequently the firing regimes in homologous regions across animal species might be similar. We analyzed neuronal spike trains recorded from behaving mice, rats, cats, and monkeys. The firing regularity differed systematically, with differences across regions in one species being greater than the differences in similar areas across species. Neuronal firing was consistently most regular in motor areas, nearly random in visual and prefrontal/medial prefrontal cortical areas, and bursting in the hippocampus in all animals examined. This suggests that firing regularity (or irregularity) plays a key role in neural computation in each functional subdivision, depending on the types of information being carried.Key words: firing irregularity/regularity; interspecies similarity; neuronal firing pattern; neuronal firing regime Significance StatementBy analyzing neuronal spike trains recorded from mice, rats, cats, and monkeys, we found that different brain regions have intrinsically different firing regimes that are more similar in homologous areas across species than across areas in one species. Because different regions in the brain are specialized for different functions, the present finding suggests that the different activity regimes of neurons are important for supporting different functions, so that appropriate neuronal codes can be used for different modalities.

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The temporal correlation hypothesis proposes that cortical neurons engage in synchronized activity, thus configuring a general mechanism to account for a range of cognitive processes from perceptual binding to consciousness. However, most studies supporting this hypothesis have only provided correlational, but not causal evidence. Here, we used electrical microstimulation of the visual and somatosensory cortices of the rat in both hemispheres, to test whether rats could discriminate synchronous versus asynchronous patterns of stimulation applied to the same cortical sites. To disambiguate synchrony from other related parameters, our experiments independently manipulated the rate and intensity of stimulation, the spatial locations of stimulation, the exact temporal sequence of stimulation patterns, and the degree of synchrony across stimulation sites. We found that rats reliably distinguished between 2 microstimulation patterns, differing in the spatial arrangement of cortical sites stimulated synchronously. Also, their performance was proportional to the level of synchrony in the microstimulation patterns. We demonstrated that rats can recognize artificial current patterns containing precise synchronization features, thus providing the first direct evidence that artificial synchronous activity can guide behavior. Such precise temporal information can be used as feedback signals in machine interface arrangements.

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