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Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition.

ABSTRACT: Neurons recruited for local computations exhibit rhythmic activity at gamma frequencies. The amplitude and frequency of these oscillations are continuously modulated depending on stimulus and behavioral state. This modulation is believed to crucially control information flow across cortical areas. Here we report that in the rat hippocampus gamma oscillation amplitude and frequency vary rapidly, from one cycle to the next. Strikingly, the amplitude of one oscillation predicts the interval to the next. Using in vivo and in vitro whole-cell recordings, we identify the underlying mechanism. We show that cycle-by-cycle fluctuations in amplitude reflect changes in synaptic excitation spanning over an order of magnitude. Despite these rapid variations, synaptic excitation is immediately and proportionally counterbalanced by inhibition. These rapid adjustments in inhibition instantaneously modulate oscillation frequency. So, by rapidly balancing excitation with inhibition, the hippocampal network is able to swiftly modulate gamma oscillations over a wide band of frequencies.

SUBMITTER: Atallah BV

PROVIDER: S-EPMC2702525 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition.

Atallah Bassam V BV Scanziani Massimo M

Neuron 20090501 4

Neurons recruited for local computations exhibit rhythmic activity at gamma frequencies. The amplitude and frequency of these oscillations are continuously modulated depending on stimulus and behavioral state. This modulation is believed to crucially control information flow across cortical areas. Here we report that in the rat hippocampus gamma oscillation amplitude and frequency vary rapidly, from one cycle to the next. Strikingly, the amplitude of one oscillation predicts the interval to the ...[more]

PMID: 19477157

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Project description:A time-varying magnetic field can cause unpleasant peripheral nerve stimulation (PNS) when the maximum excursion of the magnetic field (ΔB) is above a frequency-dependent threshold level [P. Mansfield and P. R. Harvey, Magn. Reson. Med. 29, 746-758 (1993)]. Clinical and research magnetic resonance imaging (MRI) gradient systems have been designed to avoid such bioeffects by adhering to regulations and guidelines established on the basis of clinical trials. Those trials, generally employing sinusoidal waveforms, tested human responses to magnetic fields at frequencies between 0.5 and 10 kHz [W. Irnich and F. Schmitt, Magn. Reson. Med. 33, 619-623 (1995), T. F. Budinger et al., J. Comput. Assist. Tomogr. 15, 909-914 (1991), and D. J. Schaefer et al., J. Magn. Reson. Imaging 12, 20-29 (2000)]. PNS thresholds for frequencies higher than 10 kHz had been extrapolated, using physiological models [J. P. Reilly et al., IEEE Trans. Biomed. Eng. BME-32(12), 1001-1011 (1985)]. The present study provides experimental data on human PNS thresholds to oscillating magnetic field stimulation from 2 to 183 kHz. Sinusoidal waveforms were employed for several reasons: (1) to facilitate comparison with earlier reports that used sine waves, (2) because prior designers of fast gradient hardware for generalized waveforms (e.g., including trapezoidal pulses) have employed quarter-sine-wave resonant circuits to reduce the rise- and fall-times of pulse waveforms, and (3) because sinusoids are often used in fast pulse sequences (e.g., spiral scans) [S. Nowak, U.S. patent 5,245,287 (14 September 1993) and K. F. King and D. J. Schaefer, J. Magn. Reson. Imaging 12, 164-170 (2000)].An IRB-approved prospective clinical trial was performed, involving 26 adults, in which one wrist was exposed to decaying sinusoidal magnetic field pulses at frequencies from 2 to 183 kHz and amplitudes up to 0.4 T. Sham exposures (i.e., with no magnetic fields) were applied to all subjects.For 0.4 T pulses at 2, 25, 59, 101, and 183 kHz, stimulation was reported by 22 (84.6%), 24 (92.3%), 15 (57.7%), 2 (7.7%), and 1 (3.8%) subjects, respectively.The probability of PNS due to brief biphasic time-varying sinusoidal magnetic fields with magnetic excursions up to 0.4 T is shown to decrease significantly at and above 101 kHz. This phenomenon may have particular uses in dynamic scenarios (e.g., cardiac imaging) and in studying processes with short decay times (e.g., electron paramagnetic resonance imaging, bone and solids imaging). The study suggests the possibility of new designs for human and preclinical MRI systems that may be useful in clinical practice and scientific research.

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Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition.

Publications

Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition.

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