Glutamatergic Retinal Waves.

Daniel Kerschensteiner

doi:10.3389/fncir.2016.00038

Abstract

Spontaneous activity patterns propagate through many parts of the developing nervous system and shape the wiring of emerging circuits. Prior to vision, waves of activity originating in the retina propagate through the lateral geniculate nucleus (LGN) of the thalamus to primary visual cortex (V1). Retinal waves have been shown to instruct the wiring of ganglion cell axons in LGN and of thalamocortical axons in V1 via correlation-based plasticity rules. Across species, retinal waves mature in three stereotypic stages (I–III), in which distinct circuit mechanisms give rise to unique activity patterns that serve specific functions in visual system refinement. Here, I review insights into the patterns, mechanisms, and functions of stage III retinal waves, which rely on glutamatergic signaling. As glutamatergic waves spread across the retina, neighboring ganglion cells with opposite light responses (ON vs. OFF) are activated sequentially. Recent studies identified lateral excitatory networks in the inner retina that generate and propagate glutamatergic waves, and vertical inhibitory networks that desynchronize the activity of ON and OFF cells in the wavefront. Stage III wave activity patterns may help segregate axons of ON and OFF ganglion cells in the LGN, and could contribute to the emergence of orientation selectivity in V1.

Highlights

This suggests that glutamatergic retinal waves are relayed through the early visual system up to V1
In the exploration of waves, stage III ganglion cell activity was shown to rely on glutamatergic input (Wong et al, 2000); subsequently, bipolar cells were identified as the source of this input (Blankenship et al, 2009)
AII amacrine cells, which are gap-junctionally coupled to ON cone bipolar cells (Lin et al, 2005; Marc et al, 2014), and which at maturity can generate rhythmic bursting (Cembrowski et al, 2012), do not function as pacemakers during glutamatergic waves (Firl et al, 2015). Together these findings suggest that the lateral excitatory networks that propagate glutamatergic retinal waves initiate them by amplifying coincident fluctuations in the membrane potential of nearby ON cone bipolar and/or amacrine cells

Summary

Daniel Kerschensteiner*

Departments of Ophthalmology and Visual Sciences, Neuroscience, and Biomedical Engineering, Hope Center for Neurological Diseases, Washington University School of Medicine, Saint Louis, MO, USA. Waves seem to have emerged as a source of patterned activity in species that refine ganglion cell projections while visually deprived inside a shell or womb (Demas et al, 2012). Consistent with this idea, waves have been found in all amniotes tested, but not in amphibians, which use vision to find food and avoid predators as soon as ganglion cell axons reach their targets (Holt and Harris, 1983; Demas et al, 2012). An excellent review of earlier work in ferrets, chickens, and turtles can be found here (Wong, 1999)

PATTERNS OF GLUTAMATERGIC RETINAL WAVES

MECHANISMS OF GLUTAMATERGIC RETINAL WAVES

FUNCTIONS OF GLUTAMATERGIC RETINAL WAVES

SUMMARY