Statistical Wiring of Thalamic Receptive Fields Optimizes Spatial Sampling of the Retinal Image

Abstract

Summary It is widely assumed that mosaics of retinal ganglion cells establish the optimal representation of visual space. However, relay cells in the visual thalamus often receive convergent input from several retinal afferents and, in cat, outnumber ganglion cells. To explore how the thalamus transforms the retinal image, we built a model of the retinothalamic circuit using experimental data and simple wiring rules. The model shows how the thalamus might form a resampled map of visual space with the potential to facilitate detection of stimulus position in the presence of sensor noise. Bayesian decoding conducted with the model provides support for this scenario. Despite its benefits, however, resampling introduces image blur, thus impairing edge perception. Whole-cell recordings obtained in vivo suggest that this problem is mitigated by arrangements of excitation and inhibition within the receptive field that effectively boost contrast borders, much like strategies used in digital image processing.

The Fuzzy Logic of Network Connectivity in Mouse Visual Thalamus

“…We would expect such a range of patterns could produce TC responses that vary based on type or combinations of types of innervating synapses, the size of receptive field sizes (as a result of the number of different RGCs converging on them), and receptive field shape (as a result of the bias in the orientation of their dendritic arbors). Such mixing should produce a neurons with a wider range of spatial and temporal response properties than present in retinal ganglion cells (Alonso et al, 2006; Martinez et al, 2014; Marshel et al, 2014). The idea of an ordered peripheral sensory network that gives rise to diverse combinations of connectivity in the next stage of processing has also been described in drosophila where anatomically and functionally well-defined olfactory glomeruli generate a more mixed and random input organization in the mushroom body (Caron et al, 2013).…”

Functional Convergence at the Retinogeniculate Synapse

“…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. However, these studies were performed from postnatal day (P)21–42, when experience-dependent functional rewiring of the circuit and RGC axon retraction and pruning is still occurring (Hong et al, 2014).…”

The multifunctional lateral geniculate nucleus

“…Dubin and Cleland, 1977;Lindstrom, 1982;Mastronarde, 1987b;Blitz and Regehr, 2005;Lindstrom and Wrobel, 2011;Vigeland et al, 2013). In the second, a retinal collateral of one sign makes synaptic contact with an inhibitory interneuron, which then makes synaptic contract with a relay cell of the opposite sign (Mastronarde, 1987b;Wang et al, 2011;Martinez et al, 2014). The former version creates temporal diversity and a type of LGN neuron that does not exist in the retina (the lagged cell; Mastronarde, 1987a,b), whereas the latter enhances the surround and is a form of lateral inhibition.…”