Abstract
The On-Off direction-selective ganglion cell (DSGC) in mammalian retinas responds most strongly to a stimulus moving in a specific direction. The DSGC initiates spikes in its dendritic tree, which are thought to propagate to the soma with high probability. Both dendritic and somatic spikes in the DSGC display strong directional tuning, whereas somatic PSPs (postsynaptic potentials) are only weakly directional, indicating that spike generation includes marked enhancement of the directional signal. We used a realistic computational model based on anatomical and physiological measurements to determine the source of the enhancement. Our results indicate that the DSGC dendritic tree is partitioned into separate electrotonic regions, each summing its local excitatory and inhibitory synaptic inputs to initiate spikes. Within each local region the local spike threshold nonlinearly amplifies the preferred response over the null response on the basis of PSP amplitude. Using inhibitory conductances previously measured in DSGCs, the simulation results showed that inhibition is only sufficient to prevent spike initiation and cannot affect spike propagation. Therefore, inhibition will only act locally within the dendritic arbor. We identified the role of three mechanisms that generate directional selectivity (DS) in the local dendritic regions. First, a mechanism for DS intrinsic to the dendritic structure of the DSGC enhances DS on the null side of the cell's dendritic tree and weakens it on the preferred side. Second, spatially offset postsynaptic inhibition generates robust DS in the isolated dendritic tips but weak DS near the soma. Third, presynaptic DS is apparently necessary because it is more robust across the dendritic tree. The pre- and postsynaptic mechanisms together can overcome the local intrinsic DS. These local dendritic mechanisms can perform independent nonlinear computations to make a decision, and there could be analogous mechanisms within cortical circuitry.
Highlights
The On-Off direction-selective ganglion cell (DSGC) of the mammalian retina spikes vigorously to moving stimuli, but only weakly to stationary light spots
On the null side of the dendritic tree where the intrinsic directional selectivity (DS) of the distal dendrite agreed with the presynaptic DS, the directional difference of the postsynaptic potentials (PSPs) was 2-fold or more that observed without presynaptic DS (Figure 10a,c,c,g), On the pref side of the dendritic tree, the results showed that the presynaptic mechanism can override the intrinsic DS, producing a directional difference in the evoked PSPs opposite to the local intrinsic DS signal (Figure 10b,f,d,h)
Because the findings presented here predict that dendritic isolation within the DSGC is an important biophysical factor for generating its directional selectivity, we explored how the DS response was affected by changes in the space constant of the dendritic tree
Summary
The On-Off direction-selective ganglion cell (DSGC) of the mammalian retina spikes vigorously to moving stimuli, but only weakly to stationary light spots It responds most strongly over a limited range of stimulus directions, and the direction producing the maximal response is called the ‘‘preferred’’ direction, while a stimulus moving in the opposite direction, called the ‘‘null’’ direction, produces little or no response [1]. The leading edge of a bright bar crossing the receptive field will produce a transient Onresponse, and, if the bar is wide relative to the dendritic extent and the speed low enough, the trailing-edge will produce a distinct, temporally separate Off-response In their original description of the DSGC, Barlow and Levick [2] noted that direction-selective spike output was produced for stimuli that covered only a small fraction of the dendritic arbor. These observations suggest that some type of local dendritic processing could provide the basis for the proposed subunits
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