Early postnatal development of visual function in ganglion cells of the cat retina

1. Spontaneous and visually evoked action potentials were recorded from single retinal ganglion cells in superfused retina-eyecups prepared from cats between postnatal day 5 (P5) and adulthood. The development of functional responses was studied quantitatively with contrast-modulated spots and sinusoidal grating stimuli. Some functionally characterized cells were impaled and injected intracellularly with horseradish peroxidase to permit direct structure-function comparisons during the period of synaptogenesis and the expression of transient morphological features. 2. Around the time of eye opening at postnatal day 7-postnatal day 10, the spontaneous discharge of ganglion cells was characterized by bursts of action potentials separated by periods of no activity lasting up to tens of seconds. This "burst-type" pattern gradually changed to a more regular spontaneous discharge during the first 2-3 postnatal wk. The burst-type discharge was completely blocked by 10 mM Mg2+, but was largely unaffected by bath application the excitatory amino acid receptor antagonist 6-cyano-7-nitroquinoxaline-2,3- dione at concentrations that eliminated both spontaneous and light-driven activity of cells that had developed a regular spontaneous discharge. DL-2-amino-7-phosphonoheptanoic acid, a competitive antagonist of the N-methyl-D-aspartate (NMDA) receptor, also had little effect on the burst-type discharge but did block the depolarizing effects of exogenous NMDA. These results demonstrate that the burst-type spontaneous discharge is a calcium-dependent process but probably is not mediated by synapses utilizing receptors for excitatory amino acids. 3. On P5, a minority of ganglion cells responded to a light stimulus delivered to the retina at the electrode tip. The percentage of responsive cells increased over time so that all cells responded by P10. During this transition period, the light responses were often weak, fatigued with repeated stimulation, and displayed poor temporal resolution. There was a rapid increase in the briskness of the response to a standard light stimulus during the second through fourth postnatal weeks. However, cells that responded sluggishly to visual stimulation were observed at all ages studied. 4. Both ON- and OFF-type receptive field (RF) centers were observed in approximately equal numbers as soon as the light response developed, and the proportion of the two types was independent of age. Three percent (10/342) of visually responsive ganglion cells had ON-OFF RFs, and the incidence of this type also appeared to be invariant with age.(ABSTRACT TRUNCATED AT 400 WORDS)