Impact of Acute Visual Experience on Development of LGN Receptive Fields in the Ferret.

Selectivity for direction of motion is a key feature of primary visual cortical neurons. Visual experience is required for direction selectivity in carnivore and primate visual cortex, but the circuit mechanisms of its formation remain incompletely understood. Here, we examined how developing lateral geniculate nucleus (LGN) neurons may contribute to cortical direction selectivity. Using in vivo electrophysiology techniques, we examined LGN receptive field properties of visually naive female ferrets before and after exposure to 6 h of motion stimuli to assess the effect of acute visual experience on LGN cell development. We found that acute experience with motion stimuli did not significantly affect the weak orientation or direction selectivity of LGN neurons. In addition, we found that neither latency nor sustainedness or transience of LGN neurons significantly changed with acute experience. These results suggest that the direction selectivity that emerges in cortex after acute experience is computed in cortex and cannot be explained by changes in LGN cells.SIGNIFICANCE STATEMENT The development of typical neural circuitry requires experience-independent and experience-dependent factors. In the visual cortex of carnivores and primates, selectivity for motion arises as a result of experience, but we do not understand whether the major brain area that sits between the retina and the visual cortex-the lateral geniculate nucleus of the thalamus-also participates. Here, we found that lateral geniculate neurons do not exhibit changes as a result of several hours of visual experience with moving stimuli at a time when visual cortical neurons undergo a rapid change. We conclude that lateral geniculate neurons do not participate in this plasticity and that changes in cortex are likely responsible for the development of direction selectivity in carnivores and primates.

Paired Feed-Forward Excitation With Delayed Inhibition Allows High Frequency Computations Across Brain Regions.

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.