Amacrine cell interactions underlying the response to change in the tiger salamander retina

Abstract

The neural circuitry and pharmacology underlying transient signal formation at the bipolar-amacrine cell interface were studied. Synaptic currents were measured with whole cell patch clamp in retinal slices. Cell types were identified with Lucifer yellow staining. Activity was initiated with puffs of kainate of known time course and spatial spread delivered at bipolar dendrites. OFF bipolar cells responded to kainate with a sustained inward current, but ON bipolar cells were silent. Two types of amacrine cell were found: (1) narrow field cells, with processes that extended laterally less than 200 microns, responding with a sustained inward current, and (2) wide field cells, with processes that extended laterally by up to 1 mm, responding with a brief transient inward current followed by a more sustained outward current. We pharmacologically dissected the synaptic interactions underlying the transient current in the wide field amacrine cell. In the presence of 5-aminovaleric acid (AVA), the time course of this transient current was increased so that it resembled the response of bipolar cells. Because AVA is a GABAB antagonist, it appears to block an opposing signal that truncates the sustained excitatory bipolar input, thereby generating the transient. GABAB specificity is confirmed by (1) block of the transient inward current by baclofen, a GABAB agonist, and (2) block of the baclofen effect by AVA. The site of GABAB action appears to be presynaptic to the amacrine cell membrane because neither baclofen nor AVA, in combination with picrotoxin, had a direct effect at the amacrine cell membrane. GABAB receptors are often found at presynaptic terminals where they modulate calcium or potassium conductances. It has been shown that bipolar cell terminals receive a GABAergic synaptic input (Vaughn et al., 1981; Wu et al., 1981; Tachibana and Kaneko, 1987). The narrow field sustained-responding amacrine cells appear to be GABAergic (Werblin et al., 1988). This suggests that transient activity measured in wide field amacrine cells is formed at a population of bipolar cell terminals by GABAergic feedback from narrow field amacrine cells at GABAB receptors.

Morphological and Functional Organization of ON and OFF Pathways in the Adult Newt Retina

“…Yang et al, (1991) have addressed this issue in tiger salamander retina and analyzed the retinal slice preparation by GABA immunostaining of Lucifer-yellow filling cells after recording photocurrents with whole-cell voltageclamp techniques. They identified GABA-ir ON amacrine cells with processes ramifying in sublamina b, ON-OFF amacrine cells with processes ramifying in both sublaminae a and b, and further predicted the existence of GABA-ir OFF type amacrine cells ramifying in sublamina a from a result obtained in other study (Maguire et al, 1989).…”

“…Also, bipolar cell terminals receive a GABAergic input (Marc et al, 1978;Vallerga, 1981;Wu et al, 1981). Thus, Transient bipolar cells may receive chloride-mediated inhibition at both light onset and offset, and much of this inhibition may be generated by ON-OFF amacrine cells, which ramify in both sublamina a and sublamina b (Lasansky, 1992;Maguire et al, 1989;Wu et al, 2000).…”

Optic Nerve Signals in a Neuromorphic Chip I: Outer and Inner Retina Models

“…WA, which receives excitation from both ON and OFF BT and inhibition from both ON and OFF NA, modulates presynaptic feedback inhibition from NA to BT. We use a large membrane capacitance to model the NA's slow, sustained, response, which leads to a less sustained response at the BT through presynaptic inhibition [18]. Push-pull inhibition is realized by a third set of amacrine cells in our model and is implemented by the ON-OFF BC circuit.…”

Temporal Contrast Adaptation in Salamander Bipolar Cells

“…3) indicates that contrast adaptation is mediated after signals are transferred to the bipolar cell. The experiments described below tested several possible mechanisms: (1) voltageactivated conductances in the bipolar soma (Mao et al, 1998); (2) amacrine feedback to the bipolar synaptic terminal (Maguire et al, 1989); (3) horizontal cell input to the bipolar dendrites (Mangel, 1991); and (4) Ca 2ϩ -dependent mechanisms in the bipolar dendrites (Shiells and Falk, 1999;Nawy, 2000).…”

“…Amacrine feedback was suppressed with picrotoxin and strychnine, inhibitors of the GABA (Maguire et al, 1989) and glycine (Maple and Wu, 1998;Cook et al, 2000) receptors on the bipolar synaptic terminal. A substantial increase in the amplitude of the light responses of amacrine and ganglion cells confirmed that that picrotoxin and strychnine were effective in altering inhibition from amacrine cells (data not shown).…”