Inhibition-based rhythms: experimental and mathematical observations on network dynamics

Abstract

An increasingly large body of data exists which demonstrates that oscillations of frequency 12᎐80 Hz are a consequence of, or are inextricably linked to, the behaviour of inhibitory interneurons in the central nervous system. Ž . Ž . Ž . This frequency range covers the EEG bands beta 1 12᎐20 Hz , beta 2 20᎐30 Hz and gamma 30᎐80 Hz . The pharmacological profile of both spontaneous and sensory-evoked EEG potentials reveals a very strong influence on Ž these rhythms by drugs which have direct effects on GABA receptor-mediated synaptic transmission general A .Ž . anaesthetics, sedativerhypnotics or indirect effects on inhibitory neuronal function opiates, ketamine . In addition, a number of experimental models of, in particular, gamma-frequency oscillations, have revealed both common denominators for oscillation generation and function, and subtle differences in network dynamics between the different frequency ranges. Powerful computer and mathematical modelling techniques based around both clinical and experimental observations have recently provided invaluable insight into the behaviour of large networks of interconnected neurons. In particular, the mechanistic profile of oscillations generated as an emergent property of such networks, and the mathematical derivation of this complex phenomenon have much to contribute to our understanding of how and why neurons oscillate. This review will provide the reader with a brief outline of the basic properties of inhibition-based oscillations in the CNS by combining research from laboratory models, large-scale neuronal network simulations, and mathematical analysis. ᮊ 2000 Elsevier Science B.V. All rights reserved.

Gamma oscillations as a mechanism for selective information transmission

“…With the shorter time constant, the neuron behaves more like a coincidence detector and tends to respond better to synchronized input (Azouz and Gray 2000;Kuhn et al 2004), thereby greatly amplifying the advantage of a more coherent excitatory input A over a less coherent competitor B. Regarding the PING mechanism Kopell 2003, 2005;Whittington et al 2000), a synchronized gamma frequency train A of excitatory input pulses triggers synchronous spike volleys of the I-cells, which then synchronize the E-cells by inhibitory spike volleys. The timing of the inhibition from the inhibitory neurons after the spike volleys of a coherent stimulus A to the excitatory neurons decreases the contribution of a competing, less coherent pulse train B that is uncorrelated with the more coherent stimulus A (Börgers and Kopell 2008).…”

“…In the literature, a particular role has been attributed to the "PING" (Pyramidal-Interneuronal Network Gamma) mechanism (Whittington et al 2000;Kopell 2003, 2005) in the context of gamma rhythms, which arise from the interaction between excitatory pyramidal cells (E-cells) and inhibitory interneurons (I-cells). The underlying mechanism is that spikes of the I-cells inhibit and thereby synchronize the E-cells, and that spike volleys of the E-cells trigger synchronous spike volleys of the I-cells.…”

“…The second factor relates to the role of inhibition (Börgers et al 2010). One way to generate periodic inhibition is by the "PING" (Pyramidal Interneuronal Network Gamma) mechanism Kopell 2003, 2005;Whittington et al 2000), in which a gamma rhythm arises from the interaction between excitatory pyramidal cells (E-cells) and inhibitory interneurons (I-cells). A synchronized gamma frequency train A of excitatory input pulses triggers synchronous spike volleys of the I-cells, which then synchronize the E-cells by inhibitory spike volleys.…”

Gene–environment correlations: a review of the evidence and implications for prevention of mental illness

“…Beta rhythms reflect a balance between excitatory and inhibitory networks of nerve cells and this balance is thought to be regulated by the GABA A receptor. 85 Alcohol-dependent groups have been shown to have increased power in the beta frequency, particularly in the parietal and frontal regions of the brain. 86 Taken together, these findings suggest that specific GABA A receptor gene variants (e.g., GABRA2) are associated with central nervous system (CNS) hyper-excitability, as reflected in brain oscillation patterns and that these patterns of CNS activity may underlie the behavioral disinhibition and impulsivity that characterizes alcohol dependence and other externalizing spectrum disorders.…”

Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation

“…Furthermore, the idea of short-circuiting pyramidal cell axons in order to explain ripple oscillations goes against the established principle that the PC population activity carries highly specific representational information. A second model proposes a feedback loop among PCs and inhibitory neurons [3,1 5,28,40] similar to the mechanism proposed for gamma oscillation generation [43,44]. The problem with this scenario is that the frequency of this mechanism can not be up-scaled to the ripple range [40].…”