Ganglion cells that had complex receptive field properties, namely, On-Off and On direction-selective cells, orientation-selective cells, local edge detectors, and uniformity detectors (suppressed by contrast cells) were recorded in an isolated superfused rabbit eyecup preparation. Cells were first classified by their characteristic extracellular responses to manually controlled stimuli similar to those which have been used in previous in vivo studies. Ganglion cells were then impaled, confirmed in identity by intracellular recording, and iontophoretically injected with horseradish peroxidase for staining. Twenty-two ganglion cells, which included members of all the major classes mentioned above, were recovered from the visual streak or near periphery. All recovered cells were drawn in camera lucida from flat-mounted retinas and entered into a computer as two-dimensional stick figures; nearly all were three-dimensionally reconstructed to determine the level and manner of dendritic ramification in the inner plexiform layer (IPL). The location of ganglion cell dendrites in sublaminar regions of the IPL was found to be consistent with the hypothesis of a division of the IPL into excitatory On (proximal) and Off (distal) sublaminae, with some qualifications for particular classes. Each of the complex receptive field ganglion cell classes exhibited a distinctive three-dimensional dendritic arborization pattern uniquely associated with that physiological class.

SUJMMARY1. Micro-electrode recordings were made from rabbit retinal ganglion cells or their axons. Of particular interest were direction-selective units; the common on-off type represented 206 % of the total sample (762 units), and the on-type comprised 5 %/ of the total.2. From the large sample of direction-selective units, it was found that on-off units were maximally sensitive to only four directions of movement; these directions, in the visual field, were, roughly, anterior, superior, posterior and inferior. The on-type units were maximally sensitive to only three directions: anterior, superior and inferior.3. The direction-selective unit's responses vary with stimulus velocity; both unit types are more sensitive to velocity change than to absolute speed. On-off units respond to movement at speeds from 6'/sec to 100/sec; the on-type units responded as slowly as 30"/sec up to about 2°/sec. On-type units are clearly slow-movement detectors.4. The distribution of direction-selective units depends on the retinal locality. On-off units are more common outside the 'visual streak' (area centralis) than within it, while the reverse is true for the on-type units.5. A stimulus configuration was found which would elicit responses from on-type units when the stimulus was moved in the null direction. This 'paradoxical response' was shown to be associated with the silent receptive field surround.6. The four preferred directions of the on-off units were shown to correspond to the directions of retinal image motion produced by contractions of the four rectus eye muscles. This fact, combined with data on velocity sensitivity and retinal distribution of on-off units, suggests that the on-off units are involved in control of reflex eye movements.7. The on-off direction-selective units may provide error signals to a visual servo system which minimizes retinal image motion. This hypothesis * Present address:

No abstract

The preferred directions of 102 direction-selective ganglion cells in the rabbit retina have been determined. Cells of the "on-off" type form four nonoverlapping groups; cells of the "on" type fall into three groups. The on-off groups appear to correspond to the directions of apparent object displacement produced by contractions of the four rectus muscles. Each group of cells could, without further processing, provide the error signal for a visual servo-systerm minimizing retinal image motion.

Rabbit retinal ganglion cells with concentric receptive fields were intracellularly recorded and stained in the isolated superfused eyecup preparation to relate specific physiological response properties to dendritic morphology. Concentric ganglion cells, as traditionally defined, were those that had On or Off centers with antagonistic surrounds but lacked complex response properties such as direction or orientation selectivity. Concentric cells were classified into different groups by extracellular recordings of their On- or Off-center response sign, excitatory receptive field center size, linearity of spatial summation, and brisk vs. sluggish and transient vs. sustained responses to step changes in light intensity. The cells were then impaled, confirmed in identity during intracellular recording, and iontophoretically injected with horseradish peroxidase for histological analysis. Twenty-three concentric ganglion cells were recovered and morphometrically analyzed. Their physiological response properties were found to be related to a number of underlying two- and three-dimensional attributes of the cell's dendritic branching patterns. The dendrites of all 20 brisk concentric cells and two of the three sluggish cells were found to ramify narrowly in either the proximal or distal half of the inner plexiform layer, corresponding to whether they are On center or Off center, respectively. One of the sluggish concentric cells was found to have a more complex, partially bistratified ramification. Physiologically identified brisk-sustained-linear, brisk-transient-nonlinear, brisk-transient-linear, and at least two classes of sluggish concentric ganglion cells were stained. Each of these physiological classes appears to exhibit a distinct and identifiable dendritic branching pattern.