Functional Consequences of Neuronal Divergence Within the Retinogeniculate Pathway

Abstract

Yeh C-I, Stoelzel CR, Weng C, Alonso J-M. Functional consequences of neuronal divergence within the retinogeniculate pathway. J Neurophysiol 101: 2166 -2185, 2009. First published January 28, 2009 doi:10.1152/jn.91088.2008. The neuronal connections from the retina to the dorsal lateral geniculate nucleus (dLGN) are characterized by a high specificity. Each retinal ganglion cell diverges to connect to a small group of geniculate cells and each geniculate cell receives input from a small number of retinal ganglion cells. Consistent with the high specificity of the connections, geniculate cells sharing input from the same retinal afferent are thought to have very similar receptive fields. However, the magnitude of the receptive-field mismatches, which has not been systematically measured across the different cell types in dLGN, seems to be in contradiction with the functional anatomy of the Y visual pathway: Y retinal afferents in the cat diverge into two geniculate layers (A and C) that have Y geniculate cells (Y A and Y C ) with different receptive-field sizes, response latencies, nonlinearity of spatial summation, and contrast sensitivity. To better understand the functional consequences of retinogeniculate divergence, we recorded from pairs of geniculate cells that shared input from a common retinal afferent across layers and within the same layer in dLGN. We found that nearly all cell pairs that shared retinal input across layers had Y-type receptive fields of the same sign (i.e., both on-center) that overlapped by Ͼ70%, but frequently differed in size and response latency. The receptive-field mismatches were relatively small in value (receptive-field size ratio Ͻ5; difference in peak response Ͻ5 ms), but were robustly correlated with the strength of the synchronous firing generated by the shared retinal connections (R 2 ϭ 0.75). On average, the percentage of geniculate spikes that could be attributed to shared retinal inputs was about 10% for all cell-pair combinations studied. These results are used to provide new estimates of retinogeniculate divergence for different cell classes.

Functional Convergence at the Retinogeniculate Synapse

“…In vivo recordings that correlate spiking activity of RGC-TC neuron pairs in cats and primates report one or several dominant RGCs that drive TC neuron firing (Cleland and Levick, 1971; Hubel and Wiesel, 1961; Mastronarde, 1992; Sincich et al, 2007; Yeh et al, 2009). However, additional weaker inputs were also found in cat, and notably, most RGCs drive <50% (Range 1–82%) of the postsynaptic spiking of both X and Y neurons (Rathbun et al, 2016; Usrey et al, 1999).…”

An evolving view of retinogeniculate transmission

“…Others, however (especially those focusing on Y cells in cats), show that the contribution from individual RGCs exhibits greater variability, and the activity of a single retinal input rarely accounts for the entirety of the activity of its TC neuron partner (Hubel & Wiesel, 1961; Cleland & Levick, 1971; Cleland et al, 1971; Levick et al, 1972; Mastronarde, 1992). Interestingly, one study using paired recordings across both X- and Y-cells yielded examples of RGCs that drove as few as ~1% to as many as 82% of a TC neuron’s action potentials (Usrey et al, 1999); similar results later emerged in the Y pathway (Yeh et al, 2009; Rathbun et al, 2016; considered in detail in; Weyand, 2016). Furthermore, several studies corroborate anatomical observations of divergence, such that neurons with most closely matching receptive fields exhibit the greatest correlation among their firing patterns (Alonso et al, 1996; Usrey et al, 1998).…”

The multifunctional lateral geniculate nucleus

“…Mastronarde (1992) concluded that ~33% of Y-cells in the A-layers were single input (based on recording from retinogeniculate pairs). Based on cross-correlations of spikes among LGN pairs, Alonso and colleagues (Yeh et al, 2009) reached a number of < 10% as being single input. Robson (1993) reconstructed retinal innervation to presumptive Y-cells (Class 1; Guillery, 1966) and observed that it was common for those cells to receive from multiple retinal axons (integration) and for the axons to innervate multiple LGN cells (multiplexing).…”

“…Robson (1993) reconstructed retinal innervation to presumptive Y-cells (Class 1; Guillery, 1966) and observed that it was common for those cells to receive from multiple retinal axons (integration) and for the axons to innervate multiple LGN cells (multiplexing). It is well accepted that LGN Y-cells outside the A-layers receive converging Y-cell input and the receptive fields are much larger than any one of their retinal inputs (Kratz et al, 1978;Dreher and Sefton, 1979;Yeh et al, 2009). …”