Neuronal basis of a sensory analyser, the acridid movement detector system. III. Control of response amplitude by tonic lateral inhibition.

1. The Lobular Giant Movement Detector neurone (LGMD) of Schistocerca responds with spikes when small areas of the visual field change in luminance. Previous work has shown that changes of +/- 1 log 10 unit are enough to produce maximal ON and OFF responses. 2. Using a 5 degree test area, it is shown that the number of spikes generated by such a stimulus depends on the luminance of the surrounding area. When the surround is dark, the response is maximal; when it is brightly lit, the response is minimal. Intermediate intensities produce intermediate values of response. A X 2 change in response is produced by about 3 log 10 units change in surround intensity. 3. A bright annulus, with diameters of 10-5 degrees and 25-8 degrees, inhibits both ON and OFF responses when concentric with the 5 degree test area, but not when it is 30 degrees eccentric to the test area. The inhibitory effect shows no decrease after 4 min. 4. These results are interpreted to indicate a tonic lateral inhibitory network, sited peripherally in the optic lobe prior to the divergence of the separate ON and OFF channels found in the projection from the medulla to the LGMD. It is probably identical with that described for the lamina by previous workers.     

The monosynaptic connection: the modulating effect of opioid peptides on the plasticity of presynaptic neurons and identified synapses]

Study of opioid peptides (leucine-enkephalin and methionine-enkephalin) action on plastic properties of the system of monosynaptically connected neurones LPa7--LPa3, PPa3 and LPa8--LPa3, PPa3 was conducted in the snail brain. It has been shown that all three links in the system studied (presynaptic neurone, postsynaptic neurone and synapse) manifest one and the same type of plasticity--habituation to rhythmic stimulation. Enkephalins have a modulating action on plastic properties of the presynaptic neurone and synapse: they retard the habituation of the presynaptic neurone to intracellular stimulation and retard the development of habituation at synaptic level. However, changes in the character of postsynaptic response in the presence of enkephalins are not a direct consequence of their influence on plastic properties of the presynaptic neurone. Besides, enkephalines reduce the effectiveness of synaptic transmission in the given system: they reduce EPSP duration in the postsynaptic neurone.     

Cellular basis for the response to second-order motion cues in Y retinal ganglion cells.

We perceive motion when presented with spatiotemporal changes in contrast (second-order cue). This requires linear signals to be rectified and then summed in temporal order to compute direction. Although both operations have been attributed to cortex, rectification might occur in retina, prior to the ganglion cell. Here we show that the Y ganglion cell does indeed respond to spatiotemporal contrast modulations of a second-order motion stimulus. Responses in an OFF ganglion cell are caused by an EPSP/IPSP sequence evoked from within the dendritic field; in ON cells inhibition is indirect. Inhibitory effects, which are blocked by tetrodotoxin, clamp the response near resting potential thus preventing saturation. Apparently the computation for second-order motion can be initiated by Y cells and completed by cortical cells that sum outputs of multiple Y cells in a directionally selective manner.     

Blocking Retinal Chloride Co-Transporters KCC2 and NKCC: Impact on Direction Selective ON and OFF Responses in the Rat's Nucleus of the Optic Tract

In the present study we investigated in vivo the effects of pharmacological manipulation of retinal processing on the response properties of direction selective retinal slip cells in the nucleus of the optic tract and dorsal terminal nucleus (NOT-DTN), the key visuomotor interface in the pathway underlying the optokinetic reflex. Employing a moving visual stimulus consisting of either a large dark or light edge we could differentiate direction selective ON and OFF responses in retinal slip cells. To disclose the origin of the retinal slip cells' unexpected OFF response we selectively blocked the retinal ON channels and inactivated the visual cortex by cooling. Cortical cooling had no effect on the direction selectivity of the ON or the OFF response in NOT-DTN retinal slip cells. Blockade of the retinal ON channel with APB led to a loss of the ON and, to a lesser degree, of the OFF response and a reduction in direction selectivity. Subsequent blocking of GABA receptors in the retina with picrotoxin unmasked a vigorous albeit direction unselective OFF response in the NOT-DTN. Disturbing the retinal chloride homeostasis by intraocular injections of bumetanide or furosemide led to a loss of direction selectivity in both the NOT-DTN's ON and the OFF response due to a reduced response in the neuron's preferred direction under bumetanide as well as under furosemide and a slightly increased response in the null direction under bumetanide. Our results indicate that the direction specificity of retinal slip cells in the NOT-DTN of the rat strongly depends on direction selective retinal input which depends on intraretinal chloride homeostasis. On top of the well established input from ON center direction selective ganglion cells we could demonstrate an equally effective input from the retinal OFF system to the NOT-DTN.     

Axonal Synapses Utilize Multiple Synaptic Ribbons in the Mammalian Retina

In the mammalian retina, bipolar cells and ganglion cells which stratify in sublamina a of the inner plexiform layer (IPL) show OFF responses to light stimuli while those that stratify in sublamina b show ON responses. This functional relationship between anatomy and physiology is a key principle of retinal organization. However, there are at least three types of retinal neurons, including intrinsically photosensitive retinal ganglion cells (ipRGCs) and dopaminergic amacrine cells, which violate this principle. These cell types have light-driven ON responses, but their dendrites mainly stratify in sublamina a of the IPL, the OFF sublayer. Recent anatomical studies suggested that certain ON cone bipolar cells make axonal or ectopic synapses as they descend through sublamina a, thus providing ON input to cells which stratify in the OFF sublayer. Using immunoelectron microscopy with 3-dimensional reconstruction, we have identified axonal synapses of ON cone bipolar cells in the rabbit retina. Ten calbindin ON cone bipolar axons made en passant ribbon synapses onto amacrine or ganglion dendrites in sublamina a of the IPL. Compared to the ribbon synapses made by bipolar terminals, these axonal ribbon synapses were characterized by a broad postsynaptic element that appeared as a monad and by the presence of multiple short synaptic ribbons. These findings confirm that certain ON cone bipolar cells can provide ON input to amacrine and ganglion cells whose dendrites stratify in the OFF sublayer via axonal synapses. The monadic synapse with multiple ribbons may be a diagnostic feature of the ON cone bipolar axonal synapse in sublamina a. The presence of multiple ribbons and a broad postsynaptic density suggest these structures may be very efficient synapses. We also identified axonal inputs to ipRGCs with the architecture described above.     

Electrical advantages of dendritic spines

Many neurons receive excitatory glutamatergic input almost exclusively onto dendritic spines. In the absence of spines, the amplitudes and kinetics of excitatory postsynaptic potentials (EPSPs) at the site of synaptic input are highly variable and depend on dendritic location. We hypothesized that dendritic spines standardize the local geometry at the site of synaptic input, thereby reducing location-dependent variability of local EPSP properties. We tested this hypothesis using computational models of simplified and morphologically realistic spiny neurons that allow direct comparison of EPSPs generated on spine heads with EPSPs generated on dendritic shafts at the same dendritic locations. In all morphologies tested, spines greatly reduced location-dependent variability of local EPSP amplitude and kinetics, while having minimal impact on EPSPs measured at the soma. Spine-dependent standardization of local EPSP properties persisted across a range of physiologically relevant spine neck resistances, and in models with variable neck resistances. By reducing the variability of local EPSPs, spines standardized synaptic activation of NMDA receptors and voltage-gated calcium channels. Furthermore, spines enhanced activation of NMDA receptors and facilitated the generation of NMDA spikes and axonal action potentials in response to synaptic input. Finally, we show that dynamic regulation of spine neck geometry can preserve local EPSP properties following plasticity-driven changes in synaptic strength, but is inefficient in modifying the amplitude of EPSPs in other cellular compartments. These observations suggest that one function of dendritic spines is to standardize local EPSP properties throughout the dendritic tree, thereby allowing neurons to use similar voltage-sensitive postsynaptic mechanisms at all dendritic locations.     

Cell-type specific dendritic contacts between retinal ganglion cells during development.

The extent of a neuron's dendritic field defines the region within which information is processed. The dendritic fields of functionally distinct ON and OFF center retinal ganglion cells (RGCs) form separate mosaics across the retina. Within each mosaic, neighboring dendritic fields overlap by a constant amount, sampling the visual field with the appropriate coverage. Contact-mediated lateral inhibition between neighboring RGCs has long been thought to regulate both the extent and overlap of dendritic fields during development. Here we show that dendro-dendritic contact exists between developing RGCs and occurs in a manner that would regulate the formation of ON and OFF mosaics separately. Dye-filled neighboring ON and OFF ferret alpha RGCs were reconstructed using multiphoton microscopy. At all neonatal ages examined, we observed dendro-dendritic contacts between RGCs of the same sign (ON/ON; OFF/OFF), but never between cells of opposite signs (ON/OFF). Terminal dendrites of one cell often touched a dendrite of its neighbor as they intersected. In some instances, the distal dendrite of one cell formed a fascicle with the proximal process of its neighbor. Alpha cells did not form contacts with neighboring beta cells of the same sign. Together, these observations suggest that dendro-dendritic contact between RGCs is cell-type specific. Dendritic contacts were observed even before the alpha cell arbors were completely stratified, suggesting that cell-cell recognition may take place early in their development. For each cell type, the relative overlap of dendritic fields was constant with age, despite a two-fold increase in field area. We suggest that dendro-dendritic contacts may be sites of intercellular signaling that could regulate local extension of dendrites to maintain the relative overlap of RGCs within a mosaic during development.     

Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina

The excitatory and inhibitory inputs to directionally selective (DS) ganglion cells are themselves directionally selective. Directionality is achieved because excitation is reduced during null-direction movement along a GABAergic pathway. Inhibition is reduced during preferred-direction movement along a pathway that includes cholinergic synapses. Both excitation and inhibition are made directional by laterally offset inhibitory signals similar to the spatial offset of the direct inhibitory input to the DS cell dendrites. Thus, spatially offset lateral inhibition generates directionality at three different levels in the DS circuitry. We also found that for stimuli falling within the dendritic field, cholinergic input is delivered to the OFF but not the ON dendrites. Cholinergic pathways from outside the dendritic field reach both ON and OFF dendrites, but both of these pathways are normally inactivated by GABAergic synapses.     

Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina

ON and OFF pathways separately relay increment and decrement luminance signals from retinal bipolar cells to cortex. ON-OFF retinal ganglion cells (RGCs) are activated via synaptic inputs onto bistratified dendrites localized in the ON and OFF regions of the inner plexiform layer. Postnatal maturational processes convert bistratifying ON-OFF RGCs to monostratifying ON and OFF RGCs. Although visual deprivation influences refinement of higher visual centers, no previous studies suggest that light regulates either the development of the visual-evoked signaling in retinal ON and OFF pathways, nor pruning of bistratified RGC dendrites. We find that dark rearing blocks both the maturational loss of ON-OFF responsive RGCs and the pruning of dendrites. Thus, in retina, there is a previously unrecognized, pathway-specific maturation that is profoundly affected by visual deprivation.     

Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon

A somatodendritic gradient of Cl(-) concentration ([Cl(-)](i)) has been postulated to generate GABA-evoked responses of different polarity in retinal bipolar cells, hyperpolarizing in OFF cells with low dendritic [Cl(-)](i), and depolarizing in ON cells with high dendritic [Cl(-)](i). As glutamate released by the photoreceptors depolarizes OFF cells and hyperpolarizes ON cells, the bipolars' antagonistic receptive field (RF) could be computed by simply integrating glutamatergic inputs from the RF center and GABAergic inputs from horizontal cells in the RF surround. Using ratiometric two-photon imaging of Clomeleon, a Cl(-) indicator transgenically expressed in ON bipolar cells, we found that dendritic [Cl(-)](i) exceeds somatic [Cl(-)](i) by up to 20 mM and that GABA application can lead to Cl(-) efflux (depolarization) in these dendrites. Blockers of Cl(-) transporters reduced the somatodendritic [Cl(-)](i) gradient. Hence, our results support the idea that ON bipolar cells employ a somatodendritic [Cl(-)](i) gradient to invert GABAergic horizontal cell input.     

The development of intrinsic excitability in mouse retinal ganglion cells

Activity-dependent refinement of synaptic connections occurs throughout the developing nervous system, including the visual system. Retinal ganglion cells (RGCs) overproduce synapses then refine them in an activity-dependent manner that segregates RGC connections into multicellular patterns, such as eye-specific regions and retinotopic maps. Ferrets additionally segregate ON and OFF retinogeniculate pathways in an activity-dependent manner. It was unknown whether differences in ON versus OFF intrinsic and spontaneous activity occur in postnatal mouse. The work reported here measured the intrinsic properties and spontaneous activity of morphologically identified postnatal mouse RGCs, and tested the hypothesis that mouse ON and OFF RGCs develop differences in spontaneous activity. We found developmental changes in resting potential, action potential threshold, depolarization to threshold, action potential width, action potential patterns, and maximal firing rates. These results are consistent with the maturation of the intrinsic properties of RGCs extending through the first three postnatal weeks. However, there were no differences among mouse ON, OFF, and multistratified RGCs in intrinsic excitability, spontaneous synaptic drive or spontaneous action potential patterns. The absence of differences between ON and OFF activity patterns is unlike the differences that arise in ferrets. In contrast to the ferret, the ON and OFF target neurons in the mouse are organized in a random pattern, not layers. This supports the hypothesis that the absence of systematic differences in activity results in the nonlayered distribution of retinogeniculate connections.     

The role of dopamine and serotonin in modulating the defensive behavior of the edible snail

Dopamine application in concentration of 10(-5)-10(-6) M into saline around the snail CNS leads to decrease of excitability of LPa7 neurone which is presynaptic in relation to defensive behaviour command neurones, and to decrease of amplitude of monosynaptic excitatory postsynaptic potential (EPSP) in the command neurones elicited by intracellular stimulation of LPa7 neurone. Besides, the dopamine causes a decrease of summated EPSP amplitude in the studied neurones in response to intestinal nerve stimulation (70% in average), a change of rest potential towards hyperpolarization for 6-8 mV, a reduction of the command neurones input resistance (20% in average). The described influences can lead to a general increase of the threshold of defensive system reaction to stimulation. Dopamine action on the defensive behaviour command neurones is significantly weakened in serotonine presence. Against the dopamine background, the efficiency of serotonine influence on the value of EPSP in command neurones in response to testing stimulus is reduced. According to the obtained data, a conclusion is made that interrelation of dopamine and serotonine concentrations can be a base for formation of behaviour choice in snail.     

Information processing at a central synapse suggests a noise filter in the auditory pathway of the noctuid moth

1. The central projections of the A1 afferent were confirmed via intracellular recording and staining with Lucifer Yellow in the pterothoracic ganglion of the noctuid moths, Agrotis infusa and Apamea amputatrix (Fig. 1). Simultaneous recordings of the A1 afferent in the tympanal nerve (extracellularly) and in the pterothoracic ganglion (intracellularly) confirm the identity of the stained receptor as being the A1 cell. 2. The major postsynaptic arborizations of interneurone 501 in the pterothoracic ganglion were also demonstrated via intracellular recording and staining (Fig. 2). Simultaneous recordings of the A1 afferent (extracellularly) and neurone 501 (intracellularly) revealed that each A1 spike evokes a constant short latency EPSP in the interneurone (Fig. 2Bi). Neurone 501 receives only monaural input from the A1 afferent on its soma side as demonstrated by electrical stimulation of each afferent nerve (Fig. 2Bii). EPSPs evoked in neurone 501 by high frequency (100 Hz) electrical stimulation of the afferent nerve did not decrement (Fig. 2Biii). These data are consistent with a monosynaptic input to neurone 501 from the A1 afferent. 3. The response of neurone 501 to a sound stimulus presented at an intensity near the upper limit of its linear response range (30 ms, 16 kHz, 80 dB SPL) was a plateau-like depolarization, with tonic spiking activity which continued beyond the end of the tone. The instantaneous spike frequency of the response was as high as 800 Hz, and was maintained at above 600 Hz for the duration of the tone (Fig. 3). 4. The relationship between the instantaneous spike frequency in the A1 afferent and that recorded simultaneously in neurone 501 is linear over the entire range of A1 spike frequencies evoked by white noise sound stimuli (Fig. 4). Similarly, the relationship between instantaneous spike frequency in the A1 afferent and the mean depolarization evoked in neurone 501 is also linear for all A1 spike frequencies tested (Fig. 5). No summation of EPSPs occurred for A1 spike frequencies below 100 Hz.(ABSTRACT TRUNCATED AT 250 WORDS)     

Neural adaptation facilitates oscillatory responses to static inputs in a recurrent network of ON and OFF cells

We investigate the role of adaptation in a neural field model, composed of ON and OFF cells, with delayed all-to-all recurrent connections. As external spatially profiled inputs drive the network, ON cells receive inputs directly, while OFF cells receive an inverted image of the original signals. Via global and delayed inhibitory connections, these signals can cause the system to enter states of sustained oscillatory activity. We perform a bifurcation analysis of our model to elucidate how neural adaptation influences the ability of the network to exhibit oscillatory activity. We show that slow adaptation encourages input-induced rhythmic states by decreasing the Andronov–Hopf bifurcation threshold. We further determine how the feedback and adaptation together shape the resonant properties of the ON and OFF cell network and how this affects the response to time-periodic input. By introducing an additional frequency in the system, adaptation alters the resonance frequency by shifting the peaks where the response is maximal. We support these results with numerical experiments of the neural field model. Although developed in the context of the circuitry of the electric sense, these results are applicable to any network of spontaneously firing cells with global inhibitory feedback to themselves, in which a fraction of these cells receive external input directly, while the remaining ones receive an inverted version of this input via feedforward di-synaptic inhibition. Thus the results are relevant beyond the many sensory systems where ON and OFF cells are usually identified, and provide the backbone for understanding dynamical network effects of lateral connections and various forms of ON/OFF responses.     

The effects of stimulus area and intensity on the on/off ratio of some locust visual interneurones

The on- and off-discharges of three types of locust visual interneurones were recorded in response to luminous discs ranging in subtense from 0.4 to 25°. For the DCMD neurone there was a clear reciprocal relationship between ON and OFF, with large on- and small off-responses at 0.4°, and the reverse at 25° disc subtense. Most of the changeover from almost pure ON to almost pure OFF discharges occurred in the subtense range up to 2°, i.e. within the acceptance angle of one ommatidium or the angle between adjacent ommatidia. This behaviour was not found at low luminance levels, where ON and OFF followed parallel courses. These findings suggest the existence of strong inhibition, augmenting rapidly with increase in target subtense, as also with luminance as shown in separate experiments. For the DCMD the off-response had the characteristics of a simple rebound excitation, following a short period of light exposure.The other visual interneurones (M and S) behaved differently. They did not show reciprocity of ON and OFF, but instead their responses followed parallel courses with increase in subtense, resembling those of the DCMD at low luminance. Nonetheless, like the DCMD, they did show peaking of the on-response at certain subtenses and luminance, although at much higher levels. The inhibitory activity defining the responses of M and S neurones appeared much less effective than that associated with the DCMD. This could be due to greater complexity in their central connexions, of which nothing is known.     

Transient adaptation and sensitization in the retina of Necturus

Responses to repetitive stimulation were monitored at several retinal levels in the eyecup of the mudpuppy Necturus maculosus. When alternating sequences of low-intensity small and large spots were presented, two effects were found, which could be localized to the proximal retina: (a) response decrement (RD), in which, after the first small spot response, subsequent small spot responses are decreased in amplitude and (b) transient response enhancement (TRE), in which the first small spot response after a large spot sequence is larger than preceding or subsequent small spot responses. RD and TRE are absent or weak in sustained on or off responses (horizontal and bipolar cells, and ON and OFF ganglion cell post-stimulus time histograms (PSTH) but are particularly well developed in the on/off responses of the proximal retina (proximal negative response, M-wave, PSTHs of ON/OFF ganglion cells, and intracellular responses from on/off neurons and Muller cells). RD and TRE appear to arise from a stimulus-evoked slow depolarization in on/off neurons that interacts with the amplitude of succeeding responses. We conclude that RD and TRE are a form of neural adaptation that is largely specific to the on/off channels of the proximal retina.     

Modulation of syllable period‐selective phonotaxis by prothoracic neurones in crickets (Acheta domesticus): juvenile hormone,picrotoxin and photoinactivation of the ON1 neurones

Abstract In response to model calling songs (CSs), the phonotaxis of female Acheta domesticus ranges from being very selective to unselective. Within 15 min of nanoinjecting juvenile hormone III (JHIII) or picrotoxin (PTX) into the prothoracic ganglion, females become more selective for syllable period (SP) than in pre‐tests. Controls for JHIII experiments, including nanoinjection of acetone into the prothoracic ganglion or nanoinjection of JHIII into the metathoracic ganglion, do not influence selectivity. Similarly, nanoinjection of saline into the prothoracic ganglion and nanoinjection of PTX outside of the prothoracic ganglion does not change the overall selectivity of the female’s phonotaxis. These results indicate that circuits in the prothoracic ganglion modulate the SP‐selectivity of phonotaxis. Photoinactivating both of the ON1 prothoracic auditory interneurones in old females that were previously unselective for SP also results in greater SP‐selectivity during phonotaxis. Evidence suggesting that ON1 has this effect via its inhibitory input to L3 (another prothoracic auditory neurone) includes: photoinactivation of one ON1 neurone causes angular errors in the female’s orientation to CSs at 85 dB (above the threshold of the L3), stimulation with 60 dB CSs (above the threshold of ON1 but below the threshold of L3) does not induce errors in angular orientation, inactivation of ON1 in old crickets results in greater angular errors (85 dB stimulus) than it does when ON1 is inactivated in young females, and photoinactivation of ON1 increases the firing rate of the L3 neurone.     

Response dynamics of bullfrog ON-OFF RGCs to different stimulus durations

Stimulus duration is an important feature of visual stimulation. In the present study, response properties of bullfrog ON-OFF retinal ganglion cells (RGCs) in exposure to different visual stimulus durations were studied. By using a multi-electrode recording system, spike discharges from ON-OFF RGCs were simultaneously recorded, and the cells’ ON and OFF responses were analyzed. It was found that the ON response characteristics, including response latency, spike count, as well as correlated activity and relative latency between pair-wise cells, were modulated by different light OFF intervals, while the OFF response characteristics were modulated by different light ON durations. Stimulus information carried by the ON and OFF responses was then analyzed, and it was found that information about different light ON durations was more carried by transient OFF response, whereas information about different light OFF intervals were more carried by transient ON response. Meanwhile, more than 80 % information about stimulus durations was carried by firing rate. These results suggest that ON-OFF RGCs are sensitive to different stimulus durations, and they can efficiently encode the information about visual stimulus duration by firing rate.     

Targeting of amacrine cell neurites to appropriate synaptic laminae in the developing zebrafish retina

Cellular mechanisms underlying the precision by which neurons target their synaptic partners have largely been determined based on the study of projection neurons. By contrast, little is known about how interneurons establish their local connections in vivo. Here, we investigated how developing amacrine interneurons selectively innervate the appropriate region of the synaptic neuropil in the inner retina, the inner plexiform layer (IPL). Increases (ON) and decreases (OFF) in light intensity are processed by circuits that are structurally confined to separate ON and OFF synaptic sublaminae within the IPL. Using transgenic zebrafish in which the majority of amacrine cells express fluorescent protein, we determined that the earliest amacrine-derived neuritic plexus formed between two cell populations whose somata, at maturity, resided on opposite sides of this plexus. When we followed the behavior of individual amacrine cells over time, we discovered that they exhibited distinct patterns of structural dynamics at different stages of development. During cellular migration, amacrine cells exhibited an exuberant outgrowth of neurites that was undirected. Upon reaching the forming IPL, neurites extending towards the ganglion cell layer were relatively more stable. Importantly, when an arbor first formed, it preferentially ramified in either the inner or outer IPL corresponding to the future ON and OFF sublaminae, and maintained this stratification pattern. The specificity by which ON and OFF amacrine interneurons innervate their respective sublaminae in the IPL contrasts with that observed for projection neurons in the retina and elsewhere in the central nervous system.     

Network Oscillations Drive Correlated Spiking of ON and OFF Ganglion Cells in the rd1 Mouse Model of Retinal Degeneration

Following photoreceptor degeneration, ON and OFF retinal ganglion cells (RGCs) in the rd-1/rd-1 mouse receive rhythmic synaptic input that elicits bursts of action potentials at ∼10 Hz. To characterize the properties of this activity, RGCs were targeted for paired recording and morphological classification as either ON alpha, OFF alpha or non-alpha RGCs using two-photon imaging. Identified cell types exhibited rhythmic spike activity. Cross-correlation of spike trains recorded simultaneously from pairs of RGCs revealed that activity was correlated more strongly between alpha RGCs than between alpha and non-alpha cell pairs. Bursts of action potentials in alpha RGC pairs of the same type, i.e. two ON or two OFF cells, were in phase, while bursts in dissimilar alpha cell types, i.e. an ON and an OFF RGC, were 180 degrees out of phase. This result is consistent with RGC activity being driven by an input that provides correlated excitation to ON cells and inhibition to OFF cells. A2 amacrine cells were investigated as a candidate cellular mechanism and found to display 10 Hz oscillations in membrane voltage and current that persisted in the presence of antagonists of fast synaptic transmission and were eliminated by tetrodotoxin. Results support the conclusion that the rhythmic RGC activity originates in a presynaptic network of electrically coupled cells including A2s via a Na⁺-channel dependent mechanism. Network activity drives out of phase oscillations in ON and OFF cone bipolar cells, entraining similar frequency fluctuations in RGC spike activity over an area of retina that migrates with changes in the spatial locus of the cellular oscillator.