Morphologies of rabbit retinal ganglion cells with concentric receptive fields

Abstract

Rabbit retinal ganglion cells with concentric receptive fields were intracellularly recorded and stained in the isolated superfused eyecup preparation to relate specific physiological response properties to dendritic morphology. Concentric ganglion cells, as traditionally defined, were those that had On or Off centers with antagonistic surrounds but lacked complex response properties such as direction or orientation selectivity. Concentric cells were classified into different groups by extracellular recordings of their On- or Off-center response sign, excitatory receptive field center size, linearity of spatial summation, and brisk vs. sluggish and transient vs. sustained responses to step changes in light intensity. The cells were then impaled, confirmed in identity during intracellular recording, and iontophoretically injected with horseradish peroxidase for histological analysis. Twenty-three concentric ganglion cells were recovered and morphometrically analyzed. Their physiological response properties were found to be related to a number of underlying two- and three-dimensional attributes of the cell's dendritic branching patterns. The dendrites of all 20 brisk concentric cells and two of the three sluggish cells were found to ramify narrowly in either the proximal or distal half of the inner plexiform layer, corresponding to whether they are On center or Off center, respectively. One of the sluggish concentric cells was found to have a more complex, partially bistratified ramification. Physiologically identified brisk-sustained-linear, brisk-transient-nonlinear, brisk-transient-linear, and at least two classes of sluggish concentric ganglion cells were stained. Each of these physiological classes appears to exhibit a distinct and identifiable dendritic branching pattern.

Molecular Phenotyping of Retinal Ganglion Cells

“…Considering dye-coupling patterns (Mills and Xia, 2000;Hu and Bloomfield, 2001) and our tracing of dendrites (Fig. 11), class 1a cells are ON-center and class 9 cells are OFF-center, corresponding directly to the concentric brisk nonlinear transient cells of Amthor et al (1989a) and the Y cells of carnivores.…”

“…Rabbit ␤ homologs have small somas (Amthor et al, 1989a), excluding candidate classes 1b and 1c. Brisk sustained cells are a common cell type (Levick, 1967;Oyster et al, 1971;Amthor et al, 1989a) and should have good AMPA responses. The well patterned, frequent small cells of classes 3 and 6 seem the best candidates.…”

“…By analogy with coupling patterns of ON and OFF ␣ cells, we propose class 3 as the ON-center and class 6 as the OFF-center classes. Amthor et al (1989a) distinguished these medium-sized cells from ␣ cells with caveats. Equating briskness and high AMPA responsivity, the best matches are classes 1b (ON) and 5 (OFF).…”

Projection-Specific Characteristics of Retinal Input to the Brain

“…DS RGCs have traditionally been divided into two types based on their somatodendritic morphology, response properties, and/or axonal projections. On DS RGCs exhibit large, monostratified dendritic trees, respond preferentially to slow image motion in one of three directions, and project largely, if not entirely, to the accessory optic system (Oyster et al, 1980;Buhl and Peichl, 1986;Amthor et al, 1989). On-Off DS RGCs, in comparison, exhibit small, bistratified dendritic trees; respond preferentially to rapid visual motion in one of four directions; and innervate the SC among other structures (for review, see Vaney et al, 2012).…”

The neuron classification problem

“…Group A neuron populations are most studied and Group B least. Unfortunately, morphological and physiological classifications cannot be related directly, unlike other species (Masland, 2001a, b;Amthor et al, 1989).…”