The organization of the turtle inner retina. I. ON‐ and OFF‐center pathways

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Abstract
Intracellular recordings and dye injections of Lucifer yellow, horseradish peroxidase, or Neurobiotin were made in bipolar, amacrine, and ganglion cells of the Pseudemys turtle retina. By using a standard light‐stimulation protocol in a sample of 375 labeled neurons, we were able to identify morphological and physiological characteristics of 11 types of bipolar cell, 37 types of amacrine cell, and 24 types of ganglion cell. To make sense of these data, we have chosen to group the 72 essentially different neuron types into traditional, functionally significant pathways. In this paper we look at the neuronal types in the inner plexiform layer (IPL) in terms of their contribution to generalized luminosity responses such as sustained ON‐ or OFF‐center and transient ON‐OFF ganglion cells; in the companion paper (J. Ammermüller, J. F. Muller, and H. Kolb, 1995, J. Comp. Neurol. 358:35–62) we look at them in terms of their involvement in color opponency and directional selectivity. A functional organization of the turtle IPL into OFF sublaminae (strata 1 and 2) and ON sublaminae (strata 3, 4, and 5), as has been described for other vertebrate retinas, was quite clear for two varieties of OFF‐center bipolar cells (B4 and B5) and for all four types of sustained ON‐center bipolar cell (B1, B2, B6, and B7). Thus, we found no sustained ON‐center bipolar cell terminating in strata 1 and 2. We did, however, see three varieties of sustained OFF‐center bipolar cells (B3, B9, and Bl0) having axon terminals in strata 3–5 (the ON sublamina) in addition to their terminations in stratum 1 or 2 (the OFF sublamina). Monostratified sustained ON‐ and OFF‐center amacrine and ganglion cells rigidly obeyed the border of ON and OFF sublaminae. However, multistratified and diffuse sustained amacrine and ganglion cells could be either ON‐center or OFF‐center, and they did not strictly obey the border: such ON‐center cells always had processes in one of the ON sublaminae (strata 3–5), and the equivalent OFF‐center cells always had processes in one of the OFF sublaminae (strata 1 and 2). Monostratified transient amacrine and ganglion cells were concentrated in the middle of the IPL (around stratum 3), whereas bi‐, tri‐, or multistratified transient amacrine or ganglion cells always had processes in both the ON and the OFF sublaminae. Our findings in turtle retina confirm the general “rule” of an IPL subdivided into ON‐ and OFF‐center sublaminae, a rule that ensures that ON‐ and OFF‐center monostratified sustained amacrine and ganglion cells are driven by ON‐ and OFF‐center bipolar cell types, respectively. The bipolar, amacrine, and ganglion cells that appeax to violate the bisublaminar rule in turtle inner retina are those with multistratified morphologies. We discuss our findings in terms of structural principles underlying functional receptive field organizaton and physiological response characteristics of the multitude of cell types we have encountered in this species. The findings of this paper together with those in the following paper present the most comprehensive morphophysiological descriptions of neurons contributing to the IPL of any vertebrate retina to date.