Synchronous Bursts of Action Potentials in Ganglion Cells of the Developing Mammalian Retina

Abstract

The development of orderly connections in the mammalian visual system depends on action potentials in the optic nerve fibers, even before the retina receives visual input. In particular, it has been suggested that correlated firing of retinal ganglion cells in the same eye directs the segregation of their synaptic terminals into eye-specific layers within the lateral geniculate nucleus. Such correlations in electrical activity were found by simultaneous recording of the extracellular action potentials of up to 100 ganglion cells in the isolated retina of the newborn ferret and the fetal cat. These neurons fired spikes in nearly synchronous bursts lasting a few seconds and separated by 1 to 2 minutes of silence. Individual bursts consisted of a wave of excitation, several hundred micrometers wide, sweeping across the retina at about 100 micrometers per second. These concerted firing patterns have the appropriate spatial and temporal properties to guide the refinement of connections between the retina and the lateral geniculate nucleus.

The role of nAChR‐mediated spontaneous retinal activity in visual system development

“…This spontaneous rhythmic activity was first measured in fetal rat pups and found to be highly correlated among neighboring RGCs (Galli and Maffei, 1988). Both extracellular recording using a multielectrode array (Meister et al, 1991) and imaging of calcium transients associated with bursts of action potentials Feller et al, 1997) have revealed that these spontaneous bursts propagate from one cell to the next in a wave-like manner [ Fig. 2(A)].…”

“…In the developing visual system, a function for early spontaneous activity has been well elucidated. Before phototransduction is possible, retinal ganglion cells (RGCs) fire periodic bursts of action potentials that propagate across the RGC layer in a wave-like fashion (Meister et al, 1991). These highly correlated firing patterns, called retinal waves, occur during a brief period of development when several functional circuits are being established within the retina as well as in the retinal projections to subcortical structures (Wong et al, 1993;Wong, 1999).…”

Frontiers in Neuroscience

“…We then show that applied suction also substantially improves the quality of recordings from mouse retina, a classic example of a preparation for which MEA recordings have yielded important scientific results (Meister et al, 1991;Ryan et al, 2013). Lastly, in a demonstration experiment of their compatibility with optical recording techniques, we use an MSEA to record from the nervous system of the medicinal leech, in which a voltage-sensitive dye provides simultaneous confirmation of intracellular electrical activity.…”

“…Previous MEA experiments on retinae found the optimal electrode diameter to be 10 µm (Meister et al, 1991). Accordingly, we used the intercalated electrode design, because we found that suction pores with diameters of at least 10 µm were necessary to apply adequate suction to the preparation.…”

“…Multielectrode arrays (MEAs, Gross et al, 1977;Gross, 1979;Pine, 1980;Obien et al, 2014) have successfully been used to study a range of preparations including dissociated cortical cultures (Wagenaar et al, 2006), retinal explants (Meister et al, 1991), and hippocampal slices (Steidl et al, 2006). Obtaining strong voltage signals from most of these preparations is possible, but slices continue to pose challenges, likely because of the presence of a layer of dead cells at the surface of the slice and limited oxygenation through the slice to the living cells nearest to the array.…”