Transmission of Spike Trains at the Retinogeniculate Synapse

Abstract

Retinal spikes impinging on relay neurons in the lateral geniculate nucleus (LGN) generate synaptic potentials, which sometimes produce spikes sent to visual cortex. We examined how signal transmission is regulated in the macaque LGN by recording the retinal input to a single LGN neuron while stimulating the receptive field center with a naturalistic luminance sequence. After extracting the EPSPs, which are often partially merged with spike waveforms, we found that Ͼ95% of spikes were associated with an EPSP from a single retinal ganglion cell. Each spike within a "burst" train was generated by an EPSP, indicating that LGN bursts are inherited from retinal bursts.LGN neurons rarely fired unless at least two EPSPs summated within 40 ms. This facilitation in EPSP efficacy was followed by depression. If a spike was generated by the first EPSP in a pair, it did not alter the efficacy of the second EPSP. Hence, the timing of EPSPs arising from the primary retinal driver governs synaptic efficacy and provides the basis for successful retinogeniculate transmission.

The multifunctional lateral geniculate nucleus

“…In the monkey, the S-potential is most often attributed to originating from a single retinal ganglion cell. The S-potential receptive field matches the eccentricity and polarity of the simultaneously monitored LGN neuron, its interspike interval distribution matches that of a single retinal ganglion cell, and when S-potentials are observed, the initial slope of nearly all LGN spikes matches the initial slope of the observed S-potential (Lee et al, 1983;Kaplan and Shapley, 1984;Sincich et al, 2007). Interspike interval match is critical; the presence of an S-potential from a second retinal ganglion would yield many intervals < 1 ms (cf.…”

“…If 50 ms goes by since the last retinal EPSP, the next retinal EPSP will successfully trigger an LGN spike < 2% of the time in anesthesia (e.g. Sincich et al, 2007); in wakefulness, success occurs 13% of the time (Weyand, 2007). In that study, for 9/12 neurons, intervals at 60 ms were successful > 10% of the time, with 2 hovering around 40% efficacy.…”

“…Visual stimulation drives retinal ganglion cells at high firing rates, producing short interspike intervals. Short interspike intervals in retinal ganglion cells are much more likely to drive LGN cells than long intervals (Singer et al, 1972;Mastronarde, 1987b;Usrey et al, 1998;Levine and Cleland, 2001;Rowe and Fischer, 2001;Kara and Reid, 2003;Sincich et al, 2007;Weyand, 2007). Since spontaneous (i.e.…”

Spikes with short inter-spike intervals in frog retinal ganglion cells are more correlated with their adjacent neurons’ activities

“…Spatially, burst-like spikes are more likely to be correlated with other cells' activities (Liu et al, 2011), and correlated firing is also considered as a good way to improve the information transmission from retinal ganglion cells to their post-synaptic neurons (DeVries, 1999;Usrey et al, 1999;Sincich et al, 2007). Besides, correlated burst-like spikes represent smaller receptive fields, which contributes to detailed information encoding.…”

“…Previous studies have shown that not every retinal spike fired by RGC can evoke action potential in its postsynaptic target neuron(s) (Usrey et al, 1999;Sincich et al, 2007), and that retinal spikes with a short inter-spike interval (ISI) (generally ≤ 30 ms) are more efficient to drive corresponding lateral geniculate neurons to fire (Hirsch et al, 1998;Rowe and Fischer, 2001;Sincich et al, 2007). On the other hand, correlated firing activities were observed among RGCs (Brivanlou et al, 1998;Schneidman et al, 2006), and it was suggested that RGCs might encode visual information in a dynamic population way (Schnitzer and Meister, 2003;.…”