Masked excitatory crosstalk between the ON and OFF visual pathways in the mammalian retina

Reza Farajian, Feng Pan, Abram Akopian, Béla Völgyi, Stewart A. Bloomfield

Research output: Journal article publicationJournal articleAcademic researchpeer-review

26 Citations (Scopus)

Abstract

Non-technical summary An organizing principle of the visual system is the segregation of ON and OFF responses into parallel streams to signal light increment and decrement. This segregation begins in the retina where the output ganglion cells can be divided into ON and OFF subtypes based on their responses to light. Here we show that blockade of GABAergic inhibition reveals opposite polarity responses in ganglion cells whereby OFF cells display ON responses and ON cells display OFF responses. This crossover excitation was found in both the rabbit and mouse, indicating that it is a common synaptic mechanism in the mammalian retina. Overall, these results challenge the idea that light increment and decrement is signalled by different visual pathways. Moreover, our findings suggest that release of inhibition under certain light conditions can enable single ganglion cells to carry both ON and OFF signals, thereby allowing additional information to be propagated across the limited bandwidth of the optic nerve. A fundamental organizing feature of the visual system is the segregation of ON and OFF responses into parallel streams to signal light increment and decrement. However, we found that blockade of GABAergic inhibition unmasks robust ON responses in OFF α-ganglion cells (α-GCs). These ON responses had the same centre-mediated structure as the classic OFF responses of OFF α-GCs, but were abolished following disruption of the ON pathway with l-AP4. Experiments showed that both GABAAand GABACreceptors are involved in the masking inhibition of this ON response, located at presynaptic inhibitory synapses on bipolar cell axon terminals and possibly amacrine cell dendrites. Since the dendrites of OFF α-GCs are not positioned to receive excitatory inputs from ON bipolar cell axon terminals in sublamina-b of the inner plexiform layer (IPL), we investigated the possibility that gap junction-mediated electrical synapses made with neighbouring amacrine cells form the avenue for reception of ON signals. We found that the application of gap junction blockers eliminated the unmasked ON responses in OFF α-GCs, while the classic OFF responses remained. Furthermore, we found that amacrine cells coupled to OFF α-GCs display processes in both sublaminae of the IPL, thus forming a plausible substrate for the reception and delivery of ON signals to OFF α-GCs. Finally, using a multielectrode array, we found that masked ON and OFF signals are displayed by over one-third of ganglion cells in the rabbit and mouse retinas, suggesting that masked crossover excitation is a widespread phenomenon in the inner mammalian retina. Journal compilation
Original languageEnglish
Pages (from-to)4473-4489
Number of pages17
JournalJournal of Physiology
Volume589
Issue number18
DOIs
Publication statusPublished - 1 Sep 2011
Externally publishedYes

ASJC Scopus subject areas

  • Physiology

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