Abstract
The standard architecture of neocortex is a network with excitation and inhibition in closely maintained balance. These networks respond fast and with high precision to their inputs and they allow selective amplification of patterned signals. The stability of such networks is known to depend on balancing the strengths of positive and negative feedback. We here show that a second condition is required for stability which depends on the relative strengths and time courses of fast (AMPA) and slow (NMDA) currents in the excitatory projections. This condition also determines the response time of the network. We show that networks which respond quickly to an input are necessarily close to an oscillatory instability which resonates in the delta range. This instability explains the existence of neocortical delta oscillations and the emergence of absence epilepsy. Although cortical delta oscillations are a network-level phenomenon, we show that in non-pathological networks, individual neurons receive sufficient information to keep the network in the fast-response regime without sliding into the instability.
Highlights
It is generally accepted that the model of the brain operating as a feedforward system is incorrect
Circuitry in cortex and other brain areas constitutes a finely balanced network of strongly interacting excitatory and inhibitory neuronal populations [1,2,3]. These networks can respond to their input with high temporal precision [4,5,6], selectively amplify patterned input signals [7], transmit multiple signals simultaneously between neural assemblies embedded in large networks [8], and maintain activity on a broad range of time constants [9] including those of short-term memory [10]
Deviations from the temporal balance condition by a few percent are sufficient to move the system into a state where it oscillates in the delta range and, subsequently, becomes unstable
Summary
It is generally accepted that the model of the brain operating as a feedforward system is incorrect. Circuitry in cortex and other brain areas constitutes a finely balanced network of strongly interacting excitatory and inhibitory neuronal populations [1,2,3]. These networks can respond to their input with high temporal precision [4,5,6], selectively amplify patterned input signals [7], transmit multiple signals simultaneously between neural assemblies embedded in large networks [8], and maintain activity on a broad range of time constants [9] including those of short-term memory [10]. The impact of fast α-amino3-hydroxy-5-methyl-4-isoxazolepropionic acid, (AMPA) and slow NMDA glutamatergic currents on the relative speed of positive and negative feedback has not been previously examined
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