Opposing motion inhibits responses of direction-selective ganglion cells in the fish retina

Abstract

Inhibitory influences in receptive fields (RFs) of the fish retinal direction-selective ganglion cells (DS GCs) were investigated. Responses of the fast retinal DS GCs were recorded extracellularly from their axon terminals in the superficial layer of tectum opticum of immobilized fish. The data were collected from two cyprinid species - Carassius gibelio, a wild form of the goldfish, and the barbel fish Labeobarbus intermedius. Visual stimuli were presented to the fish on the monitor screen within a square area of stimulation occupying approximately 11 × 11° of the visual field. DS GCs were stimulated by pairs of narrow stripes moving in opposing directions. One of them entered central (responsive) area of cell receptive field (RRF) from the preferred, and the other one from the null side. Stimuli merged at center of stimulation area, and subsequently moved away from each other. It was shown that the cell response evoked by the stripe coming from the preferred side of RF was inhibited by the stimulus coming from the opposite direction. In the majority of units recorded inhibitory effect induced by the null-side stimulus was initiated in the RF periphery. As a rule, inhibitory influences sent from the RF periphery were spread across the entire central area of RF. Modifications of the inhibitory influences were investigated throughout the whole motion of paired stimuli. Evident inhibitory effects mediated from the null direction were recorded during the approach of stimuli. When stripes crossed each other and moved apart inhibition was terminated, and cell response appeared again. Null-side inhibition observed in fish DS GCs is most likely induced by starburst-like amacrine cells described in morphological studies of different fish species. Possible mechanisms underlying direction selectivity in fish DS GCs are discussed.

Direction-selective units in goldfish retina and tectum opticum — review and new aspects

“…3(b); the data processed in 164 cells]. The results of our recent experiments performed in carp, roach, and barbell¯sh Labeobarbus intermedius indicated that DS GCs of these¯shes coincided with retinal DS units of C. gibelio (Damjanović et al, 2015). Results conrming our¯ndings have been recently published by Nikolaou et al (2012).…”

“…This assumption can be supported by the fact that the gold¯sh DS units were shown to respond to a broad range of velocities of moving stimuli (from 2-30 /s) (Maximov et al, 2005b), similarly as shown for fast DS GCs of the mammalian retina (see review of Vaney et al, 2001). Direction selectivity in the¯sh DS GCs was shown to be produced by the null-side inhibition (Damjanović et al, 2015), and in this respect these units also resemble the fast DS GCs of mammals (Fried et al, 2002(Fried et al, , 2005Poznanski, 2005Poznanski, , 2010. However, it is important to note that our experiments as well as study of Nikolaou et al (2012) revealed some essential di®erences between¯sh and mammalian DS GCs.…”

“…Same as before, responses of detector GCs were recorded extracellulary from their axon terminals in the retino-recipient layer of the TO using low-impedance microelectrodes. As from the year 2003, in a series of studies we have systematically investigated the responsive properties of some hundreds of movement detectors in the retina of Carassius gibelio (wild form of gold¯sh) using the newly developed experimental setup (Maximov et al, 2005a(Maximov et al, , 2005b(Maximov et al, , 2009(Maximov et al, , 2013Damjanović et al, 2009aDamjanović et al, , 2009bDamjanović et al, , 2015. Types of di®erent movement detectors were determined on the basis of their polar diagrams (directional tuning curves).…”

“…Results of that study conrmed that the¯rst stage of cardinal direction selectivity is localized to dendrites of retinal GCs and so arguments supporting evidence in favor of the postsynaptic model were provided. DS mechanisms of¯sh retina were investigated more thoroughly only recently in the study Damjanović et al (2015). As shown in Fig.…”

On the organization of receptive fields of retinal spot detectors projecting to the fish tectum: Analogies with the local edge detectors in frogs and mammals

“…The data progressively collected over a long period of time call into question the absolute meaningfulness of the "detector сoncept." So in fish, characterized by the enormous taxonomic, ecological and ethological diversity, one and the same set of retinal feature detectors was described in the TO of all of the studied species (Cronly-Dillon, 1964;Damjanovi c, Maximova, Aliper, Maximov, & Maximov, 2015;Jacobson & Gaze, 1964;Liege & Galand, 1971;Maximov et al, 2005aMaximov et al, , 1971Zenkin & Pigarev, 1969). Furthermore, practically the same set of specialized GCs was described in retinae of various mammals (Masland, 2012;O'Brien et al, 1999;van Wyk et al, 2006;Venkataramani & Taylor, 2010).…”