The midget-parvocellular pathway of marmoset retina: a quantitative light microscopic study

The midget-parvocellular pathway in foveal retina of primates shows a "private line" (one-to-one) connectivity with cone photoreceptors. The connectivity of this pathway outside the fovea is not well understood. Here, we studied the population of OFF midget bipolar cells across the retinae of marmoset monkeys (Callithrix jacchus) by using light microscopy. Cone pedicles were labeled with peanut agglutinin, OFF midget bipolar cells were labeled with antibodies against CD15, and midget ganglion cells were retrogradely labeled from the lateral geniculate nucleus and subsequently photofilled. Each midget bipolar cell contacts a single cone in foveal retina, but outside the fovea midget bipolar cells contact multiple cones: one to two cones at 1 mm ( approximately 8 degrees); three to four cones at 3-4 mm ( approximately 25 degrees); and five or more cones beyond 6 mm (>50 degrees). Throughout this eccentricity range, all medium (M) and long (L) wavelength sensitive cones make similar number of contacts with midget bipolar cells, but short wavelength sensitive (S) cones make little or no contact. By calculating the numerical convergence between midget bipolar and midget ganglion cells, we estimate that midget ganglion cells receive input from up to 25 cones at approximately 5 degrees, and from more than 65 cones at approximately 50 degrees. No obvious differences were seen between the retinae of animals with di- or trichromatic color vision. The finding that the one-to-one connectivity is restricted to the fovea predicts that in marmosets spectral mixing of M/L cone inputs will occur peripheral to 10 degrees of visual angle.