Traveling gamma-Waves: New Insights into Coupling Processes in Visual Texture Coding
Recent experiments in awake rhesus monkeys supported the binding-by-synchronization hypothesis for neural object coding in visual cortex. They demonstrated local synchrony and perceptual modulation of rhythmic or stochastic gamma-activities (30-90 Hz), according to the rules of figure-ground seg...
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|Summary:||Recent experiments in awake rhesus monkeys supported the binding-by-synchronization hypothesis for neural object coding in visual cortex. They demonstrated local synchrony and perceptual modulation of rhythmic or stochastic gamma-activities (30-90 Hz), according to the rules of figure-ground segregation. But they have also shown that the spatial extent of gamma-synchrony is restricted to few millimeters of cortical surface. Hence, the range of gamma-synchronization in retinotopically organized visual cortex can only cover small regions of the visual field, challenging the synchronization hypothesis for larger cortical object representations. Apart from synchrony, traveling waves of neural activity were found in a variety of neural structures, frequency ranges and animal species. Observations in this area are mostly described qualitatively. Suitable analysis methods were probably not known and therefore, quantitative examinations and statistical analysis of traveling waves in conjunction with perceptual binding were not successfully carried out. The lack of appropriate analysis methods is remarkable because traveling waves do not just represent another interesting type of signal coupling. They also include the state of synchrony as a special case, commonly called standing wave. In this sense, traveling waves represent a generalized form of spatio-temporal coupling. Since the preconditions for traveling waves are less restrictive than for synchrony, they may cover larger cortical regions and, thereby, help to overcome the spatial limitations of synchrony with respect to the binding hypothesis. From this point of view, it is of interest to clarify whether neural signals of gamma-activity in monkey primary visual cortex (V1) also contain traveling gamma-waves. In order to test this hypothesis, a new single-trial analysis method for multi-channel recordings was developed, called spatio-temporal correlation (STC). It is capable of detecting and quantifying traveling waves. The reliability and validity of the STC-method as well as the significance of its results was tested on artificial and experimental data in comparison with conventional pairwise correlation methods that are typically used for synchrony detection (cross-correlation, coherence). While conventional methods fail to uncover phase coupling of waves that vary their propagation direction over time, the STC-method reveals a high accuracy of traveling wave detection. Fast changes and a high variability of the waves' propagation direction lead to a destructive superposition in the temporal and trial averaging process of the conventional methods. The reinvestigation of data from previous and new experiments of our group using the STC-method demonstrated that traveling waves often occur in the gamma-frequency band of local field potential (LFP) in monkey V1. Moreover, they show strong stimulus-dependency. Their velocities (peaking at 0.3 m/s) are similar to those of spike conduction of horizontal connections measured in V1. In particular, it can be shown that gamma-waves are most likely carried by neurons representing local features of the object surface, and that their coupling range (half-height decline about 9.5mm) exceeds the coupling range of gamma-synchronization (half-height decline about 3mm) by far. These results demonstrate that gamma-synchrony in V1 is a local manifestation of large-scale traveling waves. The coupling dynamics of traveling waves depend strongly on the continuity of the object s surface. This means that phase continuity of gamma-waves exists either inside or outside of the cortical representation of an object, but cannot cross its boundaries. This decoupling effect of gamma-waves was approximately stronger by a factor of two than that of gamma-synchrony across the object boundaries. Thus, all of the above observations indicate that traveling gamma-waves reflect the functional coupling of neurons representing the local features of an object's surface, according to the Gestalt laws of perceptual binding. In conclusion, these findings strongly suggest that phase continuity of traveling gamma-waves supports the coding of object continuity as an extension to the previously mentioned binding-by-synchronization hypothesis.|
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