Cardinal difference between the orientation-selective retinal ganglion cells projecting to the fish tectum and the orientation-selective complex cells of the mammalian striate cortex

Abstract

Responses from two types of orientation-selective units of retinal origin were recorded extracellularly from their axon terminals in the medial sublaminae of tectal retinorecipient layer of immobilized cyprinid fish Carassius gibelio. Excitatory and inhibitory interactions in the receptive field were analyzed with two narrow stripes of optimal orientation flashing synchronously, one in the center and the other in different parts of the periphery. The general pattern of results was that the influence of the remote peripheral stripe was inhibitory, irrespective of the polarity of each stripe (light or dark). In this regard, the orientation-selective ganglion cells of the fish retina differ from the classical orientation-selective complex cells of the mammalian cortex, where the remote paired stripes of the opposite polarity (one light and one dark) interact in a facilitatory fashion. The consequence of these differences may be a weaker lateral inhibition in the latter case in response to stimulation by periodic gratings, which may contribute to a better spatial frequency tuning in the visual cortex.

Orientation-Selective Retinal Circuits in Vertebrates

“…After the initial discovery of orientation-selective cells in the retinae of pigeon ( Maturana and Frenk, 1963 ) and rabbit ( Levick, 1967 ), retinal orientation selectivity has since been reported in a multitude of other vertebrate species. These include macaque ( Passaglia et al, 2002 ), cat ( Levick and Thibos, 1980 , 1982 ; Shou et al, 1995 ), mouse ( Zhao et al, 2013 ; Chen et al, 2014 ; Pearson and Kerschensteiner, 2015 ; Baden et al, 2016 ; Nath and Schwartz, 2016 , 2017 ), turtle ( Sernagor and Grzywacz, 1995 ), goldfish ( Damjanovic et al, 2009 ; Damjanovic et al, 2012 ; Johnston et al, 2014 ; Johnston and Lagnado, 2015 ), and zebrafish ( Nikolaou et al, 2012 ; Antinucci et al, 2013 , 2016b ; Lowe et al, 2013 ). The study of orientation selectivity in the vertebrate retina has been pioneered in the rabbit, where (i) both orientation-selective amacrine cells ( Bloomfield, 1991 , 1994 ; Murphy-Baum and Taylor, 2015 ) and OSGCs ( Levick, 1967 ; Amthor et al, 1989 ; Bloomfield, 1994 ; Venkataramani and Taylor, 2010 , 2016 ) were initially found, (ii) the first pharmacological experiments were performed ( Caldwell et al, 1978 ; Venkataramani and Taylor, 2010 ), and (iii) it was established that orientation and direction selectivity emerge through distinct mechanisms ( He et al, 1998 ).…”