Separability of stimulus parameter encoding by on-off directionally selective rabbit retinal ganglion cells

The ganglion cell output of the retina constitutes a bottleneck in sensory processing in that ganglion cells must encode multiple stimulus parameters in their responses. Here we investigate encoding strategies of On-Off directionally selective retinal ganglion cells (On-Off DS RGCs) in rabbits, a class of cells dedicated to representing motion. The exquisite axial discrimination of these cells to preferred vs. null direction motion is well documented: it is invariant with respect to speed, contrast, spatial configuration, spatial frequency, and motion extent. However, these cells have broad direction tuning curves and their responses also vary as a function of other parameters such as speed and contrast. In this study, we examined whether the variation in responses across multiple stimulus parameters is systematic, that is the same for all cells, and separable, such that the response to a stimulus is a product of the effects of each stimulus parameter alone. We extracellularly recorded single On-Off DS RGCs in a superfused eyecup preparation while stimulating them with moving bars. We found that spike count responses of these cells scaled as independent functions of direction, speed, and luminance. Moreover, the speed and luminance functions were common across the whole sample of cells. Based on these findings, we developed a model that accurately predicted responses of On-Off DS RGCs as products of separable functions of direction, speed, and luminance ( r = 0.98; P < 0.0001). Such a multiplicatively separable encoding strategy may simplify the decoding of these cells' outputs by the higher visual centers.

Download Full-text

Visual coding with a population of direction-selective neurons

Journal of Neurophysiology ◽

10.1152/jn.00919.2014 ◽

2015 ◽

Vol 114 (4) ◽

pp. 2485-2499 ◽

Cited By ~ 23

Author(s):

Michele Fiscella ◽

Felix Franke ◽

Karl Farrow ◽

Jan Müller ◽

Botond Roska ◽

...

Keyword(s):

Microelectrode Array ◽

Ganglion Cells ◽

Tuning Curve ◽

Real Data ◽

Cell Types ◽

Average Error ◽

Retinal Ganglion ◽

Motion Direction ◽

Tuning Curves ◽

Stimulus Parameters

The brain decodes the visual scene from the action potentials of ∼20 retinal ganglion cell types. Among the retinal ganglion cells, direction-selective ganglion cells (DSGCs) encode motion direction. Several studies have focused on the encoding or decoding of motion direction by recording multiunit activity, mainly in the visual cortex. In this study, we simultaneously recorded from all four types of ON-OFF DSGCs of the rabbit retina using a microelectronics-based high-density microelectrode array (HDMEA) and decoded their concerted activity using probabilistic and linear decoders. Furthermore, we investigated how the modification of stimulus parameters (velocity, size, angle of moving object) and the use of different tuning curve fits influenced decoding precision. Finally, we simulated ON-OFF DSGC activity, based on real data, in order to understand how tuning curve widths and the angular distribution of the cells' preferred directions influence decoding performance. We found that probabilistic decoding strategies outperformed, on average, linear methods and that decoding precision was robust to changes in stimulus parameters such as velocity. The removal of noise correlations among cells, by random shuffling trials, caused a drop in decoding precision. Moreover, we found that tuning curves are broad in order to minimize large errors at the expense of a higher average error, and that the retinal direction-selective system would not substantially benefit, on average, from having more than four types of ON-OFF DSGCs or from a perfect alignment of the cells' preferred directions.

Download Full-text

Selectivity for Multiple Stimulus Features in Retinal Ganglion Cells

Journal of Neurophysiology ◽

10.1152/jn.00995.2005 ◽

2006 ◽

Vol 96 (5) ◽

pp. 2724-2738 ◽

Cited By ~ 94

Author(s):

Adrienne L. Fairhall ◽

C. Andrew Burlingame ◽

Ramesh Narasimhan ◽

Robert A. Harris ◽

Jason L. Puchalla ◽

...

Keyword(s):

Ganglion Cell ◽

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Electrode Array ◽

Retinal Ganglion ◽

Temporal Features ◽

Multiple Stimulus ◽

Feature Selectivity ◽

Small Set ◽

Stimulus Features

Under normal viewing conditions, retinal ganglion cells transmit to the brain an encoded version of the visual world. The retina parcels the visual scene into an array of spatiotemporal features, and each ganglion cell conveys information about a small set of these features. We study the temporal features represented by salamander retinal ganglion cells by stimulating with dynamic spatially uniform flicker and recording responses using a multi-electrode array. While standard reverse correlation methods determine a single stimulus feature—the spike-triggered average—multiple features can be relevant to spike generation. We apply covariance analysis to determine the set of features to which each ganglion cell is sensitive. Using this approach, we found that salamander ganglion cells represent a rich vocabulary of different features of a temporally modulated visual stimulus. Individual ganglion cells were sensitive to at least two and sometimes as many as six features in the stimulus. While a fraction of the cells can be described by a filter-and-fire cascade model, many cells have feature selectivity that has not previously been reported. These reverse models were able to account for 80–100% of the information encoded by ganglion cells.

Download Full-text