Neuronal interactions between primary and secondary visual cortical areas are important for visual processing, but the spatiotemporal patterns of the interaction are not well understood. We used voltage-sensitive dye imaging to visualize neuronal activity in rat visual cortex and found visually evoked waves propagating from V1 to other visual areas. A primary wave originated in the monocular area of V1 and was "compressed" when propagating to V2. A reflected wave initiated after compression and propagated backward into V1. The compression occurred at the V1/V2 border, and local GABAA inhibition is important for the compression. The compression/reflection pattern provides a two-phase modulation: V1 is first depolarized by the primary wave, and then V1 and V2 are simultaneously depolarized by the reflected and primary waves, respectively. The compression/reflection pattern only occurred for evoked waves and not for spontaneous waves, suggesting that it is organized by an internal mechanism associated with visual processing.
Summary Although spiral waves are ubiquitous features of nature, and have been observed in many biological systems, their existence and potential function in mammalian cerebral cortex remains uncertain. Using voltage-sensitive dye imaging, we found that spiral waves occur frequently in the neocortex in vivo, both during pharmacologically induced oscillations and during sleep-like states. While their lifespan is limited, spiral waves can modify ongoing cortical activity by influencing oscillation frequencies and spatial coherence, and by reducing amplitude in the area surrounding the spiral phase singularity. During sleep-like states, the rate of occurrence of spiral waves varies greatly depending on brain states. These results support the hypothesis that spiral waves, as an emergent activity pattern, can organize and modulate cortical population activity on the mesoscopic scale and may contribute to both normal cortical processing and to pathological patterns of activity such as those found in epilepsy.
The development of voltage-sensitive dyes (VSD) and fast optical imaging techniques have brought us a new tool for examining spatiotemporal patterns of population neuronal activity in the neocortex. Propagating waves have been observed during almost every type of cortical processing examined by VSD imaging or electrode arrays. These waves provide subthreshold depolarization to individual neurons and increase their spiking probability. Therefore, the propagation of the waves sets up a spatiotemporal framework for increased excitability in neuronal populations, which can help to determine when and where the neurons are likely to fire. In this review, first discussed is propagating waves observed in various systems and possible mechanisms for generating and sustaining these waves. Then discussed are wave dynamics as an emergent behavior of the population activity that can, in turn, influence the activity of individual neurons. The functions of spontaneous and sensoryevoked waves remain to be explored. An important next step will be to examine the interaction between dynamics of propagating waves and functions in the cortex, and to verify if cortical processing can be modified when these waves are altered.
We describe methods to achieve high sensitivity in voltage-sensitive dye (VSD) imaging from rat barrel and visual cortices in vivo with the use of a blue dye RH1691 and a high dynamic range imaging device (photodiode array). With an improved staining protocol and an off-line procedure to remove pulsation artifact, the sensitivity of VSD recording is comparable with that of local field potential recording from the same location. With this sensitivity, one can record from approximately 500 individual detectors, each covering an area of cortical tissue 160 microm in diameter (total imaging field approximately 4 mm in diameter) and a temporal resolution of 1,600 frames/s, without multiple-trial averaging. We can record 80-100 trials of intermittent 10-s trials from each imaging field before the VSD signal reduces to one half of its initial amplitude because of bleaching and wash-out. Taken together, the methods described in this report provide a useful tool for visualizing evoked and spontaneous waves from rodent cortex.
Population activity in the cortex is poorly understood. In this report we use voltage-sensitive dye imaging to examine the spatiotemporal patterns of a 7-10 Hz oscillation in neocortical slices from rat somatosensory areas. This oscillation appeared as a component of spontaneous epochs when the preparation was bathed in low [Mg] artificial CSF (ACSF) (Silva et al., 1991). Each epoch started with a synchronized spike, and 3-200 cycles of oscillation emerged afterward. Voltage-sensitive dye imaging revealed that the oscillations in the local field potential recordings were actually caused by a propagating population activation. This activation propagated in a relatively uniform size (not expanding). We call this confined, propagating activation a "dynamic ensemble." During each oscillation cycle, one (occasionally two) dynamic ensemble(s) appeared in the slice and was sustained for 60-200 msec. Dynamic ensembles propagated at approximately 30 mm/sec; the activity could propagate in both directions in cortical slices. The propagation consisted in part of "jumps," the locations of which were not fixed. Dynamic ensembles were distinguishable from the epileptiform spikes that occurred in low [Mg] ACSF. Population events similar to dynamic ensembles were also evoked under conditions of unaltered excitability (slice in normal ACSF) by electrical stimulation that activated a low density of neurons in a large area. Our data suggest that self-sustained, spatially confined, and propagating dynamic ensembles might be related to the epoch oscillations in somatosensory cortex seen in vivo (Nicolelis et al., 1995) and thus resemble one form of population activation in the neocortex.
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