Different Modes of Visual Integration in the Lateral Geniculate Nucleus Revealed by Single-Cell-Initiated Transsynaptic Tracing

Abstract

SummaryThe thalamus receives sensory input from different circuits in the periphery. How these sensory channels are integrated at the level of single thalamic cells is not well understood. We performed targeted single-cell-initiated transsynaptic tracing to label the retinal ganglion cells that provide input to individual principal cells in the mouse lateral geniculate nucleus (LGN). We identified three modes of sensory integration by single LGN cells. In the first, 1–5 ganglion cells of mostly the same type converged from one eye, indicating a relay mode. In the second, 6–36 ganglion cells of different types converged from one eye, revealing a combination mode. In the third, up to 91 ganglion cells converged from both eyes, revealing a binocular combination mode in which functionally specialized ipsilateral inputs joined broadly distributed contralateral inputs. Thus, the LGN employs at least three modes of visual input integration, each exhibiting different degrees of specialization.

Functional Convergence at the Retinogeniculate Synapse

“…We report functional retinogeniculate convergence that is greater than previously appreciated in mice (Chen and Regehr, 2000; Jaubert-Miazza et al, 2005; Lee et al, 2014; Stevens et al, 2007), but well below recent estimates from EM connectomics and retrograde rabies tracing studies of the mouse dLGN (40–91 RGC inputs: Morgan et al, 2016; Rompani et al, 2017). This discrepancy may reflect the natural progression of functional refinement between the ages of P9-60, when synapse elimination precedes axon retraction by many weeks (Chen and Regehr, 2000; Hong et al, 2014).…”

“…This discrepancy may reflect the natural progression of functional refinement between the ages of P9-60, when synapse elimination precedes axon retraction by many weeks (Chen and Regehr, 2000; Hong et al, 2014). Regional differences in binocular (Rompani et al, 2017) and monocular (present study) dLGN zones studied may also explain the inconsistency in numbers. Furthermore, Morgan et al (2016) point out that they may overestimate convergence by a factor of 2 or 3 due to potential axon branching at the level of the OT.…”

“…Using rabies tracing, Rompani et al, (2017) detected convergence of putative contacts from anatomically distinct RGCs. Whether these contacts are functional is still not known, but the observation suggests that converging inputs of different RGC subtypes may generate novel receptive field features in dLGN, adding a new dimension to thalamic processing.…”

“…Recent anatomical studies in mice using novel large-scale connectomics and retrograde viral tracing have challenged this view of retinogeniculate (RG) functional organization, showing that up to 91 RGCs may converge onto single TC neurons (Hammer et al, 2015; Morgan et al, 2016; Rompani et al, 2017). Such extensive RG convergence challenges existing models of RG function (Alonso et al, 2006; Martinez et al, 2014; Usrey and Alitto, 2015), and suggests significant thalamic processing and sensory integration of visual information.…”

Mouse dLGN receives input from a diverse population of retinal ganglion cells with limited convergence

“…Given the functional diversity of RGCs 20 and the complex input patterns of dLGN neurons 21 , one would expect an at least similarly rich functional representation in mouse dLGN. In contrast, the majority of mouse dLGN neurons has been reported to have circularly symmetric RFs and is believed to perform linear spatial summation 22,23 , similar to results in primates 24 .…”