Abstract
Neural synchronization is a mechanism whereby functionally specific brain regions establish transient networks for perception, cognition, and action. Direct addition of weak noise (fast random fluctuations) to various neural systems enhances synchronization through the mechanism of stochastic resonance (SR). Moreover, SR also occurs in human perception, cognition, and action. Perception, cognition, and action are closely correlated with, and may depend upon, synchronized oscillations within specialized brain networks. We tested the hypothesis that SR-mediated neural synchronization occurs within and between functionally relevant brain areas and thus could be responsible for behavioral SR. We measured the 40-Hz transient response of the human auditory cortex to brief pure tones. This response arises when the ongoing, random-phase, 40-Hz activity of a group of tuned neurons in the auditory cortex becomes synchronized in response to the onset of an above-threshold sound at its “preferred” frequency. We presented a stream of near-threshold standard sounds in various levels of added broadband noise and measured subjects' 40-Hz response to the standards in a deviant-detection paradigm using high-density EEG. We used independent component analysis and dipole fitting to locate neural sources of the 40-Hz response in bilateral auditory cortex, left posterior cingulate cortex and left superior frontal gyrus. We found that added noise enhanced the 40-Hz response in all these areas. Moreover, added noise also increased the synchronization between these regions in alpha and gamma frequency bands both during and after the 40-Hz response. Our results demonstrate neural SR in several functionally specific brain regions, including areas not traditionally thought to contribute to the auditory 40-Hz transient response. In addition, we demonstrated SR in the synchronization between these brain regions. Thus, both intra- and inter-regional synchronization of neural activity are facilitated by the addition of moderate amounts of random noise. Because the noise levels in the brain fluctuate with arousal system activity, particularly across sleep-wake cycles, optimal neural noise levels, and thus SR, could be involved in optimizing the formation of task-relevant brain networks at several scales under normal conditions.
Highlights
Neural synchronization is a putative mechanism whereby brain regions subserving specific functions communicate for the purpose of establishing transient networks that accomplish perception, cognition, and action [1,2]
The results reported here pertain to these four common clusters, whose characteristics are described in Table 1 and whose equivalent dipole locations in the brain are illustrated in the left column of Figure 2
We have presented a set of results that establish the existence of stochastic resonance (SR) effects both for the 40-Hz transient auditory response of the brain to near-threshold sound stimuli, implying effects on intraregional neural synchronization, and for the synchronization of oscillations in several brain regions involved in processing the neural representations of these sounds
Summary
Neural synchronization is a putative mechanism whereby brain regions subserving specific functions communicate for the purpose of establishing transient networks that accomplish perception, cognition, and action [1,2]. We describe several different modes of action of SR in the brain, both as enhancing local neural synchronization responsible for initial stimulus processing and indexed by local changes in spectral power in various frequency bands, as well as enhancing stochastic phase locking between distant brain regions cooperating in a network to manage processing of the effects of external stimuli. These results imply that SR-mediated neural synchronization is a general mechanism of brain functioning
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