The fundamental plan of the retina
Richard H. Masland
Howard Hughes Medical Institute, Wellman 429, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02114, USA
© 2001 Nature Publishing Group http://neurosci.nature.com
Correspondence should be addressed to R.M.(firstname.lastname@example.org)
The retina, like many other central nervous system structures, contains a huge diversity of neuronal types. Mammalian retinas contain approximately 55 distinct cell types, each with a different function. The census of cell types is nearing completion, as the development of quantitative methods makes it possible to be reasonably confident that few additional types exist. Although much remainsto be learned, the fundamental structural principles are now becoming clear. They give a bottom-up view of the strategies used in the retina’s processing of visual information and suggest new questions for physiological experiments and modeling.
A simple concept of the retina’s function—lateral inhibition by horizontal and amacrine cells, a direct pathway mediated by bipolar cells—is part ofthe everyday canon of neurobiology. In reality, the retina is a more complex and more subtle structure than the textbooks imply. This is of course true also for other structures of the central nervous system—such as the hippocampus or cortex—where a similar mismatch exists between a simple iconic physiology and the facts of the biological structure. Here I make an initial attempt to come to gripswith the real retina, to encompass the system’s actual cellular complexity. Neuroanatomical studies have reached a milestone. The identification and classification of retinal neurons (Fig. 1), begun more than 100 years ago by Santiago Ramon y Cajal, is nearing completion—the first time that this has been accomplished for any significantly complex structure of the mammalian CNS. This statement ispossible because much of the recent work on retinal cell populations has been quantitative. Staining cells as whole populations permits comparison of their numerical frequency. More importantly, when the number of cells of a general class (such as amacrine cells) is known, one can then determine when the identified types add up to the class total 1–4. Much detail remains to be learned, and a fewadditional cell types are sure to be discovered. However, we now know at least that no large cell populations remain unidentified, that there are no major pieces ‘missing’ within the retina’s machinery5. Unexpectedly, for most mammals, the numbers of bipolar and amacrine cells are distributed fairly evenly among the different types. This differs from initial impressions, which were much influenced byearly studies in primates. The primate fovea is anomalous in being dominated numerically by a single type of retinal ganglion cell, with an associated, specialized type of bipolar cell (see below). In other mammalian retinas, and away from the fovea in primates, individual bipolar, amacrine and ganglion cell types are numerically distributed in a more level way. Although variations certainly exist(generally, there are fewer wide-field than narrow-field neurons), there are no dominant types. In other words, the retina is not composed of a few major players surrounded by a diverse cast of minor ones. Instead, it consists of many parallel, anatomically equipotent microcircuits. How can this awesome list of cell types be sorted? What unifying principles might allow us to conceive of theretina more
nature neuroscience • volume 4 no 9 • september 2001
simply? From the work of many laboratories6–11, the fundamental backbone of the retina’s structural organization has come into view. It reinforces certain principles learned from physiological experiments, and suggests new questions for further ones. Here I review the retina’s structure and point out some unresolved functional...