Correlated firing among major ganglion cell types in primate retina

Systems Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, CA, USA.
The Journal of Physiology (Impact Factor: 5.04). 10/2010; 589(Pt 1):75-86. DOI: 10.1113/jphysiol.2010.193888
Source: PubMed


This paper examines the correlated firing among multiple ganglion cell types in the retina. For many years it has been known that ganglion cells exhibit a tendency to fire simultaneously more or less frequently than would be predicted by chance. However, the particular patterns of correlated activity in the primate retina have been unclear. Here we reveal systematic, distance-dependent correlations between different ganglion cell types. For the most part, the patterns of activity are consistent with a model in which noise in cone photoreceptors propagates through common retinal circuitry, creating correlations among ganglion cell signals.
Retinal ganglion cells exhibit substantial correlated firing: a tendency to fire nearly synchronously at rates different from those expected by chance. These correlations suggest that network interactions significantly shape the visual signal transmitted from the eye to the brain. This study describes the degree and structure of correlated firing among the major ganglion cell types in primate retina. Correlated firing among ON and OFF parasol, ON and OFF midget, and small bistratified cells, which together constitute roughly 75% of the input to higher visual areas, was studied using large-scale multi-electrode recordings. Correlated firing in the presence of constant, spatially uniform illumination exhibited characteristic strength, time course and polarity within and across cell types. Pairs of nearby cells with the same light response polarity were positively correlated; cells with the opposite polarity were negatively correlated. The strength of correlated firing declined systematically with distance for each cell type, in proportion to the degree of receptive field overlap. The pattern of correlated firing across cell types was similar at photopic and scotopic light levels, although additional slow correlations were present at scotopic light levels. Similar results were also observed in two other retinal ganglion cell types. Most of these observations are consistent with the hypothesis that shared noise from photoreceptors is the dominant cause of correlated firing. Surprisingly, small bistratified cells, which receive ON input from S cones, fired synchronously with ON parasol and midget cells, which receive ON input primarily from L and M cones. Collectively, these results provide an overview of correlated firing across cell types in the primate retina, and constraints on the underlying mechanisms.

Download full-text


Available from: Greg D Field
  • Source
    • "t al . , 2002 , 2004 ) , amphibian ( salamander : Brivanlou et al . , 1998 ) , and various mammalian retinas ( Mastronarde , 1983a , b , c ; DeVries , 1999 ; Hu and Bloomfield , 2003 ; Schnitzer and Meister , 2003 ; Schubert et al . , 2005a , b ; Völgyi et al . , 2005 , 2009 ; Shlens et al . , 2006 ; Hoshi et al . , 2006 ; Trong and Rieke , 2008 ; Greschner et al . , 2011 ) . Ganglion cell spike synchronization has been sug - gested to encode information of the visual scene ( Meister and Berry , 1999 ; Schwartz et al . , 2007 ) to predict stimulus modulation ( Schwartz et al . , 2007 ; Schwartz and Berry , 2008 ) or to serve tem - poral binding of information or salient signaling along the visual axis ( "
    [Show abstract] [Hide abstract]
    ABSTRACT: Gap junctions connect cells in the bodies of all multicellular organisms, forming either homologous or heterologous (i.e. established between identical or different cell types, respectively) cell-to-cell contacts by utilizing identical (homotypic) or different (heterotypic) connexin protein subunits. Gap junctions in the nervous system serve electrical signaling between neurons, thus they are also called electrical synapses. Such electrical synapses are particularly abundant in the vertebrate retina where they are specialized to form links between neurons as well as glial cells. In this article, we summarize recent findings on retinal cell-to-cell coupling in different vertebrates and identify general features in the light of the evergrowing body of data. In particular, we describe and discuss tracer coupling patterns, connexin proteins, junctional conductances and modulatory processes. This multispecies comparison serves to point out that most features are remarkably conserved across the vertebrate classes, including (i) the cell types connected via electrical synapses; (ii) the connexin makeup and the conductance of each cell-to-cell contact; (iii) the probable function of each gap junction in retinal circuitry; (iv) the fact that gap junctions underlie both electrical and/or tracer coupling between glial cells. These pan-vertebrate features thus demonstrate that retinal gap junctions have changed little during the over 500 million years of vertebrate evolution. Therefore, the fundamental architecture of electrically coupled retinal circuits seems as old as the retina itself, indicating that gap junctions deeply incorporated in retinal wiring from the very beginning of the eye formation of vertebrates. In addition to hard wiring provided by fast synaptic transmitter-releasing neurons and soft wiring contributed by peptidergic, aminergic and purinergic systems, electrical coupling may serve as the 'skeleton' of lateral processing, enabling important functions such as signal averaging and synchronization.
    Full-text · Article · Jan 2013 · Progress in Retinal and Eye Research
  • Source
    • "Recordings from large populations of RGCs from the isolated macaque retina in vitro, carried out with multi-electrode arrays, have provided new information about the retinal output, beyond the properties of individual cells. In agreement with the previous work of Mastronarde (1983) on the cat retina, Greschner et al. (2011) found that cells of a given type tended to have correlated firing. The correlations declined with the retinal distance between the cells. "

    Full-text · Chapter · Jan 2013
  • Source
    • "From this mosaic we extracted the pairwise distances between the centers of the respective fields. The amount of synchronized firing between pairs of RGCs of the same type declines systematically with distance between the two cells (Mastronarde, 1983; Meister et al., 1995; De Vries, 1999; Shlens et al., 2006; Greschner, 2010). This well described behavior was used as a benchmark against which we tested the capability of the various spike train distances to assign higher values to more distant cell pairs (or lower values to more distant cell pairs in case of the correlation coefficient C). "
    [Show abstract] [Hide abstract]
    ABSTRACT: A wide variety of approaches to estimate the degree of synchrony between two or more spike trains have been proposed. One of the most recent methods is the ISI-distance which extracts information from the interspike intervals (ISIs) by evaluating the ratio of the instantaneous firing rates. In contrast to most previously proposed measures it is parameter free and time-scale independent. However, it is not well suited to track changes in synchrony that are based on spike coincidences. Here we propose the SPIKE-distance, a complementary measure which is sensitive to spike coincidences but still shares the fundamental advantages of the ISI-distance. In particular, it is easy to visualize in a time-resolved manner and can be extended to a method that is also applicable to larger sets of spike trains. We show the merit of the SPIKE-distance using both simulated and real data.
    Full-text · Article · Jan 2011 · Journal of Neuroscience Methods
Show more