Bipolar Cell Receptive Fields Research Articles

Center-surround interactions underlie bipolar cell motion sensitivity in the mouse retina.

Motion sensing is a critical aspect of vision. We studied the representation of motion in mouse retinal bipolar cells and found that some bipolar cells are radially direction selective, preferring the origin of small object motion trajectories. Using a glutamate sensor, we directly observed bipolar cells synaptic output and found that there are radial direction selective and non-selective bipolar cell types, the majority being selective, and that radial direction selectivity relies on properties of the center-surround receptive field. We used these bipolar cell receptive fields along with connectomics to design biophysical models of downstream cells. The models and additional experiments demonstrated that bipolar cells pass radial direction selective excitation to starburst amacrine cells, which contributes to their directional tuning. As bipolar cells provide excitation to most amacrine and ganglion cells, their radial direction selectivity may contribute to motion processing throughout the visual system.

Nonlinear spatial integration in retinal bipolar cells shapes the encoding of artificial and natural stimuli

SummaryThe retina dissects the visual scene into parallel information channels, which extract specific visual features through nonlinear processing. The first nonlinear stage is typically considered to occur at the output of bipolar cells, resulting from nonlinear transmitter release from synaptic terminals. In contrast, we show here that bipolar cells themselves can act as nonlinear processing elements at the level of their somatic membrane potential. Intracellular recordings from bipolar cells in the salamander retina revealed frequent nonlinear integration of visual signals within bipolar cell receptive field centers, affecting the encoding of artificial and natural stimuli. These nonlinearities provide sensitivity to spatial structure below the scale of bipolar cell receptive fields in both bipolar and downstream ganglion cells and appear to arise at the excitatory input into bipolar cells. Thus, our data suggest that nonlinear signal pooling starts earlier than previously thought: that is, at the input stage of bipolar cells.

Inhibitory components of retinal bipolar cell receptive fields are differentially modulated by dopamine D1 receptors.

During adaptation to an increase in environmental luminance, retinal signaling adjustments are mediated by the neuromodulator dopamine. Retinal dopamine is released with light and can affect center-surround receptive fields, the coupling state between neurons, and inhibitory pathways through inhibitory receptors and neurotransmitter release. While the inhibitory receptive field surround of bipolar cells becomes narrower and weaker during light adaptation, it is unknown how dopamine affects bipolar cell surrounds. If dopamine and light have similar effects, it would suggest that dopamine could be a mechanism for light-adapted changes. We tested the hypothesis that dopamine D1 receptor activation is sufficient to elicit the magnitude of light-adapted reductions in inhibitory bipolar cell surrounds. Surrounds were measured from OFF bipolar cells in dark-adapted mouse retinas while stimulating D1 receptors, which are located on bipolar, horizontal, and inhibitory amacrine cells. The D1 agonist SKF-38393 narrowed and weakened OFF bipolar cell inhibitory receptive fields but not to the same extent as with light adaptation. However, the receptive field surround reductions differed between the glycinergic and GABAergic components of the receptive field. GABAergic inhibitory strength was reduced only at the edges of the surround, while glycinergic inhibitory strength was reduced across the whole receptive field. These results expand the role of retinal dopamine to include modulation of bipolar cell receptive field surrounds. Additionally, our results suggest that D1 receptor pathways may be a mechanism for the light-adapted weakening of glycinergic surround inputs and the furthest wide-field GABAergic inputs to bipolar cells. However, remaining differences between light-adapted and D1 receptor-activated inhibition demonstrate that non-D1 receptor mechanisms are necessary to elicit the full effect of light adaptation on inhibitory surrounds.

Pannexin 1 Is Critically Involved in Feedback from Horizontal Cells to Cones.

Retinal horizontal cells (HCs) feed back negatively to cone photoreceptors and in that way generate the center/surround organization of bipolar cell receptive fields. The mechanism by which HCs inhibit photoreceptors is a matter of debate. General consensus exists that horizontal cell activity leads to the modulation of the cone Ca-current. This modulation has two components, one fast and the other slow. Several mechanisms for this modulation have been proposed: a fast ephaptic mechanism, and a slow pH mediated mechanism. Here we test the hypothesis that the slow negative feedback signal from HCs to cones is mediated by Panx1 channels expressed at the tips of the dendrites of horizontal cell. We generated zebrafish lacking Panx1 and found that the slow component of the feedback signal was strongly reduced in the mutants showing that Panx1 channels are a fundamental part of the negative feedback pathway from HCs to cones.

Dopamine Regulation of GABAA Receptors Contributes to Light/Dark Modulation of the ON-Cone Bipolar Cell Receptive Field Surround in the Retina

Cone bipolar cells are interneurons that receive synaptic input from cone photoreceptor cells and provide the output of the first synaptic layer of the retina. These cells exhibit center-surround receptive fields, a prototype of lateral inhibition between neighboring sensory cells in which stimulation of the receptive field center excites the cell whereas stimulation of the surrounding region laterally inhibits the cell. This fundamental sensory coding mechanism facilitates spatial discrimination and detection of stimulus edges. However, although it is well established that the receptive field surround is strongest when ambient or background illumination is most intense, e.g., at midday, and that the surround is minimal following maintained darkness, the synaptic mechanisms that produce and modulate the surround have not been resolved. Using electrical recording of bipolar cells under experimental conditions in which the cells exhibited surround light responses, and light and electron microscopic immunocytochemistry, we show in the rabbit retina that bright-light-induced activation of dopamine D1 receptors located on ON-center cone bipolar cell dendrites increases the expression and activity of GABAA receptors on the dendrites of the cells and that surround light responses depend on endogenous GABAA receptor activation. We also show that maintained darkness and D1 receptor blockade following maintained illumination and D1 receptor activation result in minimal GABAA receptor expression and activity and greatly diminished surrounds. Modulation of the D1/GABAA receptor signaling pathway of ON-cBC dendrites by the ambient light level facilitates detection of spatial details on bright days and large dim objects on moonless nights.

Inhibition decorrelates visual feature representations in the inner retina.

SUMMARYThe retina extracts visual features for transmission to the brain. Different types of bipolar cell split the photoreceptor input into parallel channels and provide the excitatory drive for downstream visual circuits. Anatomically and genetically, mouse bipolar cell types have been described at great detail, but a similarly deep understanding of their functional diversity is lacking. By imaging light-driven glutamate release from more than 13,000 bipolar cell axon terminals in the intact retina, we here show that bipolar cell functional diversity is generated by the interplay of dendritic excitatory inputs and axonal inhibitory inputs. The resultant centre and surround components of bipolar cell receptive fields interact to decorrelate bipolar cell output in the spatial and temporal domain. Our findings highlight the importance of inhibitory circuits in generating functionally diverse excitatory pathways and suggest that decorrelation of parallel visual pathways begins already at the second synapse of the mouse visual system.

The Synaptic and Morphological Basis of Orientation Selectivity in a Polyaxonal Amacrine Cell of the Rabbit Retina.

Much of the computational power of the retina derives from the activity of amacrine cells, a large and diverse group of GABAergic and glycinergic inhibitory interneurons. Here, we identify an ON-type orientation-selective, wide-field, polyaxonal amacrine cell (PAC) in the rabbit retina and demonstrate how its orientation selectivity arises from the structure of the dendritic arbor and the pattern of excitatory and inhibitory inputs. Excitation from ON bipolar cells and inhibition arising from the OFF pathway converge to generate a quasi-linear integration of visual signals in the receptive field center. This serves to suppress responses to high spatial frequencies, thereby improving sensitivity to larger objects and enhancing orientation selectivity. Inhibition also regulates the magnitude and time course of excitatory inputs to this PAC through serial inhibitory connections onto the presynaptic terminals of ON bipolar cells. This presynaptic inhibition is driven by graded potentials within local microcircuits, similar in extent to the size of single bipolar cell receptive fields. Additional presynaptic inhibition is generated by spiking amacrine cells on a larger spatial scale covering several hundred microns. The orientation selectivity of this PAC may be a substrate for the inhibition that mediates orientation selectivity in some types of ganglion cells. Significance statement: The retina comprises numerous excitatory and inhibitory circuits that encode specific features in the visual scene, such as orientation, contrast, or motion. Here, we identify a wide-field inhibitory neuron that responds to visual stimuli of a particular orientation, a feature selectivity that is primarily due to the elongated shape of the dendritic arbor. Integration of convergent excitatory and inhibitory inputs from the ON and OFF visual pathways suppress responses to small objects and fine textures, thus enhancing selectivity for larger objects. Feedback inhibition regulates the strength and speed of excitation on both local and wide-field spatial scales. This study demonstrates how different synaptic inputs are regulated to tune a neuron to respond to specific features in the visual scene.

Functional properties of spontaneous excitatory currents and encoding of light/dark transitions in horizontal cells of the mouse retina.

As all visual information is represented in the spatio-temporal dynamics of transmitter release from photoreceptors and the combined postsynaptic responses of second-order neurons, appropriate synaptic transfer functions are fundamental for a meaningful perception of the visual world. The functional contribution of horizontal cells to gain control and organization of bipolar and ganglion cell receptive fields can only be evaluated with an in-depth understanding of signal processing in horizontal cells. Therefore, a horizontal slice preparation of the mouse retina was established to record from horizontal cell bodies with their dendritic fields intact and receiving functional synaptic input from cone photoreceptors. Horizontal cell bodies showed spontaneous excitatory currents (spEPSCs) of monophasic and more complex multi-peak waveforms. spEPSCs were induced by quantal release of glutamate from presynaptic cones with a unitary amplitude of 3 pA. Non-stationary noise analysis revealed that spEPSCs with a monoexponential decay were mediated by 7-8 glutamate receptors with a single-channel amplitude of 1.55 pA. Responses to photopic full-field illumination were characterized by reduction of a tonic inward current or hyperpolarization, inhibition of spEPSCs, followed by a fast and transient inward current at light offset. The response to periodic dark/light transitions of different frequencies was dependent on the adaptational status of the cell with a limiting frequency of 10 Hz. Both on and off components of the light response were mediated by AMPA and kainate receptors. Detailed analysis of horizontal cell synaptic physiology is a prerequisite for understanding signal coding and processing at the photoreceptor ribbon synapse.

Extracellular ATP hydrolysis inhibits synaptic transmission by increasing ph buffering in the synaptic cleft.

Author SummaryAt the first retinal synapse, specific cells—horizontal cells (HCs)—inhibit photoreceptors and help to organize the receptive fields of another retinal cell type, bipolar cells. This synaptic interaction is crucial for visual contrast enhancement. Here we show that horizontal cells feed back to photoreceptors via a very fast ephaptic mechanism and a relatively slow mechanism. The slow mechanism requires ATP release via Pannexin 1 (Panx1) channels that are located on HC dendrites near the site where photoreceptors release the neurotransmitter glutamate to HCs and bipolar cells. The released ATP is hydrolyzed to produce AMP, phosphate groups, and protons; these phosphates and protons form a pH buffer, which acidifies the synaptic cleft. This slow acidification inhibits presynaptic calcium channels and consequently reduces the neurotransmitter release of photoreceptors. This demonstrates a new way in which ATP release can be involved in synaptic modulation. Surprisingly, the action of ATP is not purinergic but is mediated via changes in the pH buffer capacity in the synaptic cleft. Given the broad expression of Panx1 channels in the nervous system and the suggestion that Panx1 function underlies stabilization of synaptic plasticity and is needed for learning, we anticipate that this mechanism will be more widespread than just occurring at the first retinal synapse.

Cell-Specific Cre Recombinase Expression Allows Selective Ablation of Glutamate Receptors from Mouse Horizontal Cells

In the mouse retina, horizontal cells form an electrically coupled network and provide feedback signals to photoreceptors and feedforward signals to bipolar cells. Thereby, horizontal cells contribute to gain control at the first visual synapse and to the antagonistic organization of bipolar and ganglion cell receptive fields. However, the nature of horizontal cell output remains a matter of debate, just as the exact contribution of horizontal cells to center-surround antagonism. To facilitate studying horizontal cell function, we developed a knockin mouse line which allows ablating genes exclusively in horizontal cells. This knockin line expresses a Cre recombinase under the promoter of connexin57 (Cx57), a gap junction protein only expressed in horizontal cells. Consistently, in Cx57+/Cre mice, Cre recombinase is expressed in almost all horizontal cells (>99%) and no other retinal neurons. To test Cre activity, we crossbred Cx57+/Cre mice with a mouse line in which exon 11 of the coding sequence for the ionotropic glutamate receptor subunit GluA4 was flanked by two loxP sites (GluA4fl/fl). In GluA4fl/fl:Cx57+/Cre mice, GluA4 immunoreactivity was significantly reduced (∼50%) in the outer retina where horizontal cells receive photoreceptor inputs, confirming the functionality of the Cre/loxP system. Whole-cell patch-clamp recordings from isolated horizontal cell somata showed a reduction of glutamate-induced inward currents by ∼75%, suggesting that the GluA4 subunit plays a major role in mediating photoreceptor inputs. The persistent current in GluA4-deficient cells is mostly driven by AMPA and to a very small extent by kainate receptors as revealed by application of the AMPA receptor antagonist GYKI52466 and concanavalin A, a potentiator of kainate receptor-mediated currents. In summary, the Cx57+/Cre mouse line provides a versatile tool for studying horizontal cell function. GluA4fl/fl:Cx57+/Cre mice, in which horizontal cells receive less excitatory input, can thus be used to analyze the contribution of horizontal cells to retinal processing.

Lateral interactions in the outer retina.

Lateral interactions in the outer retina, particularly negative feedback from horizontal cells to cones and direct feed-forward input from horizontal cells to bipolar cells, play a number of important roles in early visual processing, such as generating center-surround receptive fields that enhance spatial discrimination. These circuits may also contribute to post-receptoral light adaptation and the generation of color opponency. In this review, we examine the contributions of horizontal cell feedback and feed-forward pathways to early visual processing. We begin by reviewing the properties of bipolar cell receptive fields, especially with respect to modulation of the bipolar receptive field surround by the ambient light level and to the contribution of horizontal cells to the surround. We then review evidence for and against three proposed mechanisms for negative feedback from horizontal cells to cones: 1) GABA release by horizontal cells, 2) ephaptic modulation of the cone pedicle membrane potential generated by currents flowing through hemigap junctions in horizontal cell dendrites, and 3) modulation of cone calcium currents (I(Ca)) by changes in synaptic cleft proton levels. We also consider evidence for the presence of direct horizontal cell feed-forward input to bipolar cells and discuss a possible role for GABA at this synapse. We summarize proposed functions of horizontal cell feedback and feed-forward pathways. Finally, we examine the mechanisms and functions of two other forms of lateral interaction in the outer retina: negative feedback from horizontal cells to rods and positive feedback from horizontal cells to cones.

Closed-Loop Measurements of Iso-Response Stimuli Reveal Dynamic Nonlinear Stimulus Integration in the Retina

Neurons often integrate information from multiple parallel signaling streams. How a neuron combines these inputs largely determines its computational role in signal processing. Experimental assessment of neuronal signal integration, however, is often confounded by cell-intrinsic nonlinear processes that arise after signal integration has taken place. To overcome this problem and determine how ganglion cells in the salamander retina integrate visual contrast over space, we used automated online analysis of recorded spike trains and closed-loop control of the visual stimuli to identify different stimulus patterns that give the same neuronal response. These iso-response stimuli revealed a threshold-quadratic transformation as a fundamental nonlinearity within the receptive field center. Moreover, for a subset of ganglion cells, the method revealed an additional dynamic nonlinearity that renders these cells particularly sensitive to spatially homogeneous stimuli. This function is shown to arise from a local inhibition-mediated dynamic gain control mechanism.

Response characteristics and receptive field widths of on-bipolar cells in the mouse retina.

Voltage-clamp and current-clamp recordings were made from bipolar cells in dark-adapted mouse retinal slices. Light-evoked responses fell into three groups corresponding to the rod bipolar cells, on-cone bipolar cells and off-cone bipolar cells. The morphology of the recorded cells confirmed this classification. Intensity-response relations were well fitted by a Michaelis saturation function with Hill coefficients of 1.15 +/- 0.11 (n = 6) for rod bipolar cells and 2.33 +/- 0.06 (n = 4) for cone inputs onto on-cone bipolar cells. In the absence of antagonists for GABA or glycine receptors, light-evoked synaptic currents for all cells displayed linear current-voltage relations that reversed near 0 mV, indicating that very little inhibition was activated under dark-adapted recording conditions. Saturating light stimuli evoked conductances of 0.81 +/- 0.56 nS (n = 4) in rod bipolar cells and 1.1 +/- 0.8 nS (n = 4) in on-cone bipolar cells. Receptive field widths were estimated by flashing a vertical light bar at various locations along the slice. Rod and on-cone bipolar cells had receptive field widths of 67 +/- 16 micrometer (n = 6) and 43 +/- 7 microm (n = 5), respectively. The maximum spatial resolution of an array of such cone bipolar cells was estimated to be 0.3 cycles deg-1, compared with a maximum resolution of 0.5 cycles deg-1 obtained from behavioural studies in mice. Our results suggest that this limit to spatial resolution could be imposed early in the visual system by the size of the bipolar cell receptive fields.

The role of retinal bipolar cell in early vision: an implication with analogue networks and regularization theory.

A linear analogue network model is proposed to describe the neuronal circuit of the outer retina consisting of cones, horizontal cells, and bipolar cells. The model reflects previous physiological findings on the spatial response properties of these neurons to dim illumination and is expressed by physiological mechanisms, i.e., membrane conductances, gap-junctional conductances, and strengths of chemical synaptic interactions. Using the model, we characterized the spatial filtering properties of the bipolar cell receptive field with the standard regularization theory, in which the early vision problems are attributed to minimization of a cost function. The cost function accompanying the present characterization is derived from the linear analogue network model, and one can gain intuitive insights on how physiological mechanisms contribute to the spatial filtering properties of the bipolar cell receptive field. We also elucidated a quantitative relation between the Laplacian of Gaussian operator and the bipolar cell receptive field. From the computational point of view, the dopaminergic modulation of the gap-junctional conductance between horizontal cells is inferred to be a suitable neural adaptation mechanism for transition between photopic and mesopic vision.

Dopaminergic modulation of visual sensitivity in man.

A large body of experimental evidence supports the hypothesis that dopamine is a functional neuromodulator at many levels of the visual system. Intrinsic dopaminergic neurons were characterized in most mammalian retina, including man. These neurons give rise to a dendritic plexus covering the retina. Thus, dopamine seems to be involved in the organization of the ganglion cell and the bipolar cell receptive fields and modulates physiological activity of photoreceptors, both processes which underlie sensitivity and spatial selectivity of visual processing in the early stage of the visual system. Moreover, few data are now available concerning the functional significance of dopaminergic modulation of visual sensitivity in man. Parkinson's disease is a specific disorder of central dopaminergic systems. Abnormalities in the pattern-evoked potentials and electroretinogram have been found in parkinsonian patients. Contrast sensitivity, a useful tool for measuring visual spatio-temporal sensitivity in man, has also been shown to be modified due to this affection. Dynamic contrast sensitivity is primarily decreased in these patients, distinguishing them from the normal aging process. Because these modifications in shape of the contrast sensitivity function are reversed by L-Dopa, and that neuroleptic administration could reproduce them in schizophrenia patients, it was suggested that dopamine might tune the contrast sensitivity function in man. We have recently shown that subcutaneous apomorphine induces changes in contrast sensitivity in healthy volunteers, which preferentially affect motion sensitivity. These dopaminergic sensitive modifications in the shape of the contrast sensitivity function might reflect a change in the range of sensitivity of the visual system, both in dynamic and spatial properties. This could be explained by a modification in the spatial and dynamic properties of the ganglion cell responses in the retina. Moreover, we suggest both from our results and from the review of the literature that human psychophysical data confirm the hypothesis that dopamine may be involved in light retinal adaptation, as light-induced and dopamine-induced modifications in the shape in the contrast sensitivity function are quite similar.

Spatial organization of the bipolar cell's receptive field in the retina of the tiger salamander.

1. The spatial properties of rods, horizontal cells and bipolar cells were studied by intracellular recording in the isolated, perfused retina of the tiger salamander, Ambystoma tigrinum. Low stimulus intensities were used in order to keep cell responses close to, or within, their linear intensity/response range. 2. Spatial properties of bipolar cell receptive fields, measured while perfusing with normal Ringer solution, were compared with those measured during exposure to agents that eliminated the bipolar cells' receptive field surround (RFS). In this way, the spatial properties of the receptive field centre (RFC) and those of the RFS could be characterized independently. 3. To a good approximation, the contribution to the horizontal cell's response of unit area of its receptive field declined exponentially with distance from the centre of the receptive field. The (apparent) length constant describing this decay was 200 microns. The one-dimensional length constant of the horizontal cell syncytium was thus 248 microns. The variation of response amplitude with the radius of a centred circular stimulus was consistent with this finding. 4. This was true also of the RFCs of bipolar cells. The one-dimensional length constant of the RFC of off-centre bipolar cells averaged 124 microns. That of the RFC of on-centre cells averaged 62 microns though values were more variable, the RFCs of some on-centre cells being comparable to those of off-centre cells. These values were independent of the class of photoreceptor driving the bipolar cell. 5. The large size of the RFCs of off-centre cells and many on-centre cells cannot by explained by light scatter within the retina or by voltage spread within the rod syncytium. We proposed that off-centre cells are tightly coupled in a syncytium. On-centre cells, on average, are less tightly coupled. 6. The spatial properties of the bipolar cell's RFS were consistent with the notion that the RFS represents a convolution of the horizontal cell's receptive field and the bipolar cell's RFC. 7. The spatial properties of bipolar cell receptive fields were reconstructed from the measured properties of their RFCs and the measured properties of horizontal cell receptive fields. Under the conditions of our experiments, the bipolar cell's response could be described by a linear difference between a component generated by the RFC and a component generated by the RFS. 8. The spatial filtering characteristics of the bipolar cells were calculated from our data.(ABSTRACT TRUNCATED AT 400 WORDS)

Structure of the receptive fields of bipolar cells in the salamander retina.

1. The receptive-field structure of bipolar cells in the salamander retina has been examined using isolated retinae from dark-adapted eyes. 2. Receptive-field mapping was carried out with a 25-microns diam spot of light whose wavelength and intensity was intended to stimulate rods rather than cones. 3. Both hyperpolarizing and depolarizing bipolar cells showed receptive fields having a single central point of maximum sensitivity from which sensitivity declined radially. Antagonistic surrounds could not be demonstrated using a small spot of light. 4. The diameter of receptive fields was found to vary between 374 and 662 micron, consistent with a single bipolar cell being effectively connected to 323-1,275 rods. 5. Lucifer yellow injections of bipolar cells revealed dendritic arbors whose greatest dimensions varied between 43 and 70 microns, consistent with a direct synaptic connection of between 10 and 24 rods to each bipolar cell. 6. We rule out signal spread within the rod network, extensive lateral ramification of rod process, nonlinearity of synaptic transmission, and light scatter, as possible explanations of large bipolar cell receptive fields. It seems likely, instead, that signals are extensively shared between bipolar cells.

Cone input to bipolar cells in the turtle retina

Action spectra were obtained by intracellular recordings from bipolar cells of the retina of turtle Pseudemys scripta. All bipolar cells responded independently to spots and annuli. Bipolar cells could be broken down into two main categories which differed in the dependence of centersurround interactions on changes in wavelength. In the first category, center-surround antagonism occurred regardless of the wavelengths used. Spectral analysis of these cells showed that both the center and surround received their major input from red cones. With chromatic adaptation, green cone input was detected in the center response of some cells. In the second category, activation of the surround was antagonistic to the center for some wavelengths and synergistic for others. These cells had a color-opponent center of the R/G type imbedded in a non-opponent surround. The surround spectral sensitivity curve could be matched by a simple linear sum of the spectral sensitivities of red-cone-dominated L 1 horizontal cells and C-R/GB horizontal cells. Theories concerning the formation of bipolar cell receptive fields are discussed. It is concluded that simple feedback from red cones to green cones via L 1 horizontal cells cannot fully account for the chromatic properties of the bipolar cells reported in this study.

Interactions of rod and cone signals in the mudpuppy retina.

Interactions between rod and cone signals in mudpuppy retinal neurones were investigated by intracellular recording. 2. The mudpuppy retina contains one kind of rod (lambda max = 525 nm) and one kind of cone (lambda max = 572 nm). The responses of receptors can be distinguished on the basis of their spectral sensitivities. 3. Rod and cone responses have different time courses of recovery and absolute sensitivities. Differences between receptor responses can be used to describe inputs to interneurones. 4. There are two spectral classes of horizontal cells: L-type and C-type. L-type cells are hyperpolarized by rods and cones in varying proportion, with some cells receiving little rod input. C-type cells are hyperpolarized by rods and depolarized by cones. 5. Bipolar cell receptive field centres receive input from cones or from rods and cones. There is no correlation between the spectral properties of centre responses and their polarity. 6. Antagonistic surrounds of bipolar cells show cone or rod and cone sensitivity. They are believed to be generated by the L-type horizontal cells. 7. Some bipolar cells exhibit chromatic interactions between cone signals in the centre and rod signals in the surround, which resemble those observed between the signals of different spectral classes of cones in species known to possess colour discrimination. 8. Amacrine and on-off ganglion cells have L-type responses showing both rod and cone sensitivity. 9. It is proposed that interactions between rod and cone signals observed in mudpuppy also exist in primate retina and are at least partially responsible for certain psychophysical observations of rod-cone interactions.

Control of retinal sensitivity. II. Lateral interactions at the outer plexi form layer.

Test stimuli, presented at the center of the bipolar cell receptive field, spanning less than 2 log units of intensity, elicit the full range of graded response. The intensity range of test stimuli that elicits the graded response depends upon the background conditions. A higher range of log test intensities is required to elicit the graded bipolar response in the presence of surround backgrounds. But surround backgrounds can also serve to unsaturate the bipolar response and thereby increase sensitivity under certain conditions. The results suggest that a second stage of sensitivity-control is mediated by the horizontal cell system at the outer plexiform layer, concatenated with the effects of adaptation in the photoreceptors.