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The Journal of Neuroscience, May 15, 1999, 19(10):3992-4010
Precisely Synchronized Oscillatory Firing Patterns Require
Electroencephalographic Activation
Suzana
Herculano-Houzel,
Matthias H. J.
Munk,
Sergio
Neuenschwander, and
Wolf
Singer
Max-Planck-Institut für Hirnforschung, 60528 Frankfurt/Main,
Germany
Neuronal response synchronization with millisecond precision has
been proposed to serve feature binding in vision and should therefore,
like visual experience, depend on central states. Here we test this
hypothesis by examining the occurrence and strength of response
synchronization in areas 17 and 18 of anesthetized cats as a function
of central states. These were assessed from the frequency content of
the electroencephalogram, low power in the and high
power in the frequency ranges (here 20-70 Hz) being considered as
a signature of activated states. We evaluated both spontaneous state
changes and transitions induced by electrical stimulation of the
mesencephalic reticular formation. During states of low central
activation, visual responses were robust but lacked signs of precise
synchronization. At intermediate levels of activation, responses became
synchronized and exhibited an oscillatory patterning in the range of
70-105 Hz. At higher levels of activation, a different pattern of
response synchronization and oscillatory modulation appeared,
oscillation frequency now being in the range of 20-65 Hz. The strength
of response synchronization and oscillatory modulation in the 20-65 Hz
range increased with further activation and was associated with a
decrease in oscillation frequency. We propose that the oscillatory
patterning in the 70-105 Hz range is attributable to oscillatory
retinothalamic input and that a minimal level of activation is
necessary for cortical neurons to follow this oscillatory pattern. In
contrast, the synchronization of responses at oscillation frequencies
in the 20-65 Hz range appears to result from intracortical synchronizing mechanisms, which become progressively more effective as
central activation increases. Surprisingly, enhanced synchronization and oscillatory modulation in the frequency range were not
associated with consistent increases in response amplitude, excluding a
simple relation between central activation and neuronal discharge rate. The fact that intracortical synchronizing mechanisms are particularly effective during states of central activation supports the hypothesis that precise synchronization of responses plays a role in sensory processing.
Key words:
synchronization; frequency oscillations; EEG; cortical activation; visual perception; thalamocortical interactions; sleep
Copyright © 1999 Society for Neuroscience 0270-6474/99/19103992-19$05.00/0
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