Spatial receptive fields in the retina and dorsal lateral geniculate nucleus of mice lacking rods and cones.

Abstract

In advanced retinal degeneration loss of rods and cones leaves melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) as the only source of visual information. ipRGCs drive non-image-forming responses (e.g., circadian photoentrainment) under such conditions but, despite projecting to the primary visual thalamus [dorsal lateral geniculate nucleus (dLGN)], do not support form vision. We wished to determine what precludes ipRGCs supporting spatial discrimination after photoreceptor loss, using a mouse model (rd/rd cl) lacking rods and cones. Using multielectrode arrays, we found that both RGCs and neurons in the dLGN of this animal have clearly delineated spatial receptive fields. In the retina, they are typically symmetrical, lack inhibitory surrounds, and have diameters in the range of 10-30° of visual space. Receptive fields in the dLGN were larger (diameters typically 30-70°) but matched the retinotopic map of the mouse dLGN. Injections of a neuroanatomical tracer (cholera toxin β-subunit) into the dLGN confirmed that retinotopic order of ganglion cell projections to the dLGN and thalamic projections to the cortex is at least superficially intact in rd/rd cl mice. However, as previously reported for deafferented ipRGCs, onset and offset of light responses have long latencies in the rd/rd cl retina and dLGN. Accordingly, dLGN neurons failed to track dynamic changes in light intensity in this animal. Our data reveal that ipRGCs can convey spatial information in advanced retinal degeneration and identify their poor temporal fidelity as the major limitation in their ability to provide information about spatial patterns under natural viewing conditions.

• Authors: Christopher A Procyk, Cyril G Eleftheriou, Riccardo Storchi, Annette E Allen, Nina Milosavljevic, Timothy M Brown, Robert J Lucas
• Journal: Journal of neurophysiology (J Neurophysiol) Vol. 114 Issue 2 Pg. 1321-30 (Aug 2015) ISSN: 1522-1598 [Electronic] United States
• PMID: 26084909 (Publication Type: Journal Article, Research Support, Non-U.S. Gov't)
• Copyright: Copyright © 2015 the American Physiological Society.

Chemical References

• Neuronal Tract-Tracers
• Rod Opsins
• melanopsin
• Cholera Toxin

Topics

• Action Potentials
• Animals
• Cholera Toxin
• Female
• Geniculate Bodies (pathology, physiology)
• Male
• Mice, Inbred C3H
• Neuroanatomical Tract-Tracing Techniques
• Neuronal Tract-Tracers
• Photic Stimulation
• Retina (physiology)
• Retinal Cone Photoreceptor Cells (pathology, physiology)
• Retinal Degeneration (physiopathology)
• Retinal Ganglion Cells (pathology, physiology)
• Retinal Rod Photoreceptor Cells (pathology, physiology)
• Rod Opsins (metabolism)
• Vision Tests
• Vision, Ocular (physiology)