Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb

PLoS Computational Biology, Oct 2009

Local field potential (LFP) oscillations are often accompanied by synchronization of activity within a widespread cerebral area. Thus, the LFP and neuronal coherence appear to be the result of a common mechanism that underlies neuronal assembly formation. We used the olfactory bulb as a model to investigate: (1) the extent to which unitary dynamics and LFP oscillations can be correlated and (2) the precision with which a model of the hypothesized underlying mechanisms can accurately explain the experimental data. For this purpose, we analyzed simultaneous recordings of mitral cell (MC) activity and LFPs in anesthetized and freely breathing rats in response to odorant stimulation. Spike trains were found to be phase-locked to the gamma oscillation at specific firing rates and to form odor-specific temporal patterns. The use of a conductance-based MC model driven by an approximately balanced excitatory-inhibitory input conductance and a relatively small inhibitory conductance that oscillated at the gamma frequency allowed us to provide one explanation of the experimental data via a mode-locking mechanism. This work sheds light on the way network and intrinsic MC properties participate in the locking of MCs to the gamma oscillation in a realistic physiological context and may result in a particular time-locked assembly. Finally, we discuss how a self-synchronization process with such entrainment properties can explain, under experimental conditions: (1) why the gamma bursts emerge transiently with a maximal amplitude position relative to the stimulus time course; (2) why the oscillations are prominent at a specific gamma frequency; and (3) why the oscillation amplitude depends on specific stimulus properties. We also discuss information processing and functional consequences derived from this mechanism.

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Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb

Buonviso N (2009) Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb. PLoS Comput Biol 5(10): e1000551. doi:10.1371/journal.pcbi.1000551 Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb Fran c¸ois O. David 0 Etienne Hugues 0 Tristan Cenier 0 Nicolas Fourcaud-Trocme´ 0 Nathalie 0 Abigail Morrison, RIKEN Brain Science Institute, Japan 0 1 Neurosciences Sensorielles , Comportement, Cognition , CNRS-Universite ́ Claude Bernard , Lyon , France , 2 Department of Information and Communication Technologies, Universitat Pompeu Fabra , Barcelona, Spain, 3 IFR 19 , Institut Fe ́de ́ratif des Neurosciences de Lyon , Lyon , France Local field potential (LFP) oscillations are often accompanied by synchronization of activity within a widespread cerebral area. Thus, the LFP and neuronal coherence appear to be the result of a common mechanism that underlies neuronal assembly formation. We used the olfactory bulb as a model to investigate: (1) the extent to which unitary dynamics and LFP oscillations can be correlated and (2) the precision with which a model of the hypothesized underlying mechanisms can accurately explain the experimental data. For this purpose, we analyzed simultaneous recordings of mitral cell (MC) activity and LFPs in anesthetized and freely breathing rats in response to odorant stimulation. Spike trains were found to be phaselocked to the gamma oscillation at specific firing rates and to form odor-specific temporal patterns. The use of a conductance-based MC model driven by an approximately balanced excitatory-inhibitory input conductance and a relatively small inhibitory conductance that oscillated at the gamma frequency allowed us to provide one explanation of the experimental data via a mode-locking mechanism. This work sheds light on the way network and intrinsic MC properties participate in the locking of MCs to the gamma oscillation in a realistic physiological context and may result in a particular time-locked assembly. Finally, we discuss how a self-synchronization process with such entrainment properties can explain, under experimental conditions: (1) why the gamma bursts emerge transiently with a maximal amplitude position relative to the stimulus time course; (2) why the oscillations are prominent at a specific gamma frequency; and (3) why the oscillation amplitude depends on specific stimulus properties. We also discuss information processing and functional consequences derived from this mechanism. - Funding: This work was funded by the CNRS and the Universite Claude Bernard-Lyon 1. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. . These authors contributed equally to this work. Introduction Recent experiments under awake conditions indicate that there is little effective spatial contrast in the firing rate of neurons in olfactory structures [ 1 ] and even in auditory primary sensory structures [ 2 ], which suggests a limited role for the mean firing rate in sensory function. In addition, it has recently been shown in the retina that the sole firing rate is not sufficient to code for behavioral performance [ 3 ]. Furthermore, the role of spike timing for plasticity [ 4 ] and coding [ 5 ] suggests that the temporal structure of neuronal activity may be crucial for perception. In particular, various functional studies have reported that fast local field potential (LFP) oscillations, particularly those in the gamma band (40–80 Hz) that correlate with perception [ 6 ] and attention [ 7 ], simultaneously induce a greater synchrony in the firing of cells, thereby having a greater impact on downstream structures [ 7 ]. In the mammalian olfactory bulb (OB), odorant stimulation induces LFP oscillations both in the gamma (40–80 Hz) and beta (15–35 Hz) ranges. There is, however, significant disparity in the reports regarding the conditions in which these oscillations are expressed. In anesthetized animals, gamma and beta LFP oscillations are odor-induced and appear alternately along the respiratory cycle, with gamma bursts specifically occurring during the inspiration/expiration (I/E) transition [ 8,9 ]. In the awake rat, gamma and beta LFP oscillations exist spontaneously, and odors evoke increases [10] or decreases [ 11 ] of amplitude in the gamma frequency range. In insects [ 5,12 ] and to a lesser extent in fish [13], spiking activity has been shown to be strongly linked to the oscillation which plays therefore a crucial role in coding. In rodents the role of these oscillation has been primarily described to reflect the experience of the animal [ 14,15 ]. Despite the findings of phase/time relationships between mitral (MC) spiking activity and the oscillation or between MC pairs [ 16–18 ], a better description of these relationships (...truncated)


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François O. David, Etienne Hugues, Tristan Cenier, Nicolas Fourcaud-Trocmé, Nathalie Buonviso. Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb, PLoS Computational Biology, 2009, 10, DOI: 10.1371/journal.pcbi.1000551