Abstract
The transmission of high frequency temporal information across brain regions is critical to perception, but the mechanisms underlying such transmission remain unclear. Long-range projection patterns across brain areas are often comprised of paired feed-forward excitation followed closely by delayed inhibition, including the thalamic triad synapse, thalamic projections to cortex, and projections within the hippocampus. Previous studies have shown that these joint projections produce a shortened period of depolarization, sharpening the timing window over which the postsynaptic neuron can fire. Here we show that these projections can facilitate the transmission of high frequency computations even at frequencies that are highly filtered by neuronal membranes. This temporal facilitation occurred over a range of synaptic parameter values, including variations in synaptic strength, synaptic time constants, short-term synaptic depression, and the delay between excitation and inhibition. Further, these projections can coordinate computations across multiple network levels, even amid ongoing local activity. We suggest that paired feed-forward excitation and inhibition provide a hybrid signal—carrying both a value and a clock-like trigger—to allow circuits to be responsive to input whenever it arrives.
Highlights
In digital electronics, computations are synchronized by the presence of a digital clock trigger signal that indicates when each digital component should examine its inputs and perform a computation
Our goal was to understand the physics of the configuration of paired feed-forward excitatory and inhibitory (FFEI) connections that are commonly observed in projections across brain regions
We found that feed-forward excitation and inhibition (FFEI) projections allowed feed-forward computations at much higher frequencies than if feed-forward excitatory (FFE) projections were employed alone
Summary
Computations are synchronized by the presence of a digital clock trigger signal that indicates when each digital component should examine its inputs and perform a computation. It allows digital circuits to have short integration times because the components do not need to consider information that has arrived at its inputs long in the past. This short integration time allows the digital circuit to operate at high temporal speeds (many computations per second). The digital clock allows synchronization of computations across different layers of digital components, because the arrival of related inputs is coordinated by the digital clock
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