The functional organization of the crayfish lamina ganglionaris

Summary

• 1. The functional properties of the multicolumnar interneurons of the crayfish lamina ganglionaris were examined by intracellular recording and the cell structures were revealed with the aid of Lucifer yellow or horseradish peroxidase iontophoresis.

• 2. The multicolumnar monopolar cell M₅ (Fig. 1) responds to a light pulse with a depolarizing compound EPSP and a burst of action potentials. Both the EPSP amplitude and the spike rate decay toward a lower level plateau in less than 200 ms after light onset. M₅ is subject to surround inhibition, which is associated with a compound IPSP and net hyperpolarization of the membrane potential. Direct depolarization of M₅ may provide a weak excitatory drive to medullary sustaining fibers (SF).

• 3. Tangenital-cell type 1 (Tan₁) (Fig. 2) has a broad expanse of neurites in the lamina (covering 10 to 15 cartridges) and a much narrower projection in the medulla (1 to 3 cartridges). The response to a light pulse (Fig. 3) has a long latency consistent with a polysynaptic receptor to Tan₁ pathway. The response consists of a nearly rectangular hyperpolarization. Light ‘off’ elicits a depolarization and a burst of impulses. The polarity of the ‘on’ response can be reversed by hyperpolarizing the membrane by 23 mV. The receptive field is broad and the intensity-response function exceeds 4 log units. Direct hyperpolarization of Tan₁ provides a strong excitatory signal to medullary SFs both in the dark and in the presence of illumination (Fig. 5). We propose that Tan₁ provides the principal steady-state excitatory drive to the SFs.

• 4. Tangential-cell type 2 (Tan₂) (Fig. 4) is distinguished from Tan₁ by the extent and shape of the lamina process, which is a vertically oriented neurite spanning most of the lamina in a single plane. Functionally, Tan₂ is similar in most respects to Tan₁ but the response latency is much shorter, comparable to that of monopolar cells.

• 5. T-cells may exhibit spontaneous impulse activity in the dark which is inhibited by a short latency hyperpolarizing light response. The receptive field, which is about 2x larger than that of the columnar monopolar cells, is correlated with a small but multicolumnar dendritic arbor in the lamina. Since T-cells are aminergic, it is possible that the amines are normally released in the dark.

• 6. A single amacrine cell was fully characterized (Fig. 7). It exhibited a short latency hyperpolarizing response to light onset and a strong depolarizing ‘off’ response. The receptive field was of intermediate dimensions (larger than that of monopolars and smaller than that of tangentials), and was subject to strong lateral inhibition. Membrane polarization excited SFs. Hyperpolarization was about twice as effective as depolarization (Fig. 7C).

• 7. A circuit diagram of the lamina and the lamina to medulla connections (Fig. 9) is proposed on the basis of our results and previous morphological studies. The results are consistent with three general hypotheses: a) all synapses in the lamina are sign-inverting; b) the lamina to medulla projections appear to be mediated by sign-inverting synapses to a single functional class of transmedullary neurons; and c) the neurons of the external chiasma constitute a hierarchy of parallel lamina to medulla pathways with receptive fields varying from 8° (nonspiking monopolar cells) to 180° (Tan₂) and response dynamics varying from purely transient (columnar monopolars) to steady state (tangential cells).