RESUMEN
In the first visual synapse of the insect compound eye, both the presynaptic and postsynaptic signals are graded, nonspiking changes in membrane voltage. The synapse exhibits tonic transmitter release (even in dark) and strong adaptation to long-lasting light backgrounds, leading to changes also in the dynamics of signal transmission. We have studied these adaptational properties of the first visual synapse of the blowfly Calliphora vicina. Investigations were done in situ by intracellular recordings from the presynaptic photoreceptors, photoreceptor axon terminals, and the postsynaptic first order visual interneurons (LMCs). The dark recovery, the shifts in intensity dependence, and the underlying processes were studied by stimulating the visual system with various adapting stimuli while observing the recovery (i.e., dark adaptation). The findings show a transient potentiation in the postsynaptic responses after intense light adaptation, and the underlying mechanisms seem to be the changes in the equilibrium potential of the transmitter-gated conductance (chloride) of the postsynaptic neurons. The potentiation by itself serves as a mechanism that after light adaptation rapidly recovers the sensitivity loss of the visual system. However, this kind of mechanism, being an intrinsic property of graded potential transmission, may be quite widespread among graded synapses, and the phenomenon demonstrates that functional plasticity is also a property of graded synaptic transmission.
Asunto(s)
Dípteros/fisiología , Células Fotorreceptoras de Invertebrados/citología , Células Fotorreceptoras de Invertebrados/fisiología , Sinapsis/fisiología , Visión Ocular/fisiología , Adaptación Ocular/fisiología , Animales , Axones/fisiología , Canales de Cloruro/fisiología , Cloruros/metabolismo , Adaptación a la Oscuridad/fisiología , Conductividad Eléctrica , Potenciales de la Membrana/fisiología , Neuronas Aferentes/fisiología , Neuronas Aferentes/ultraestructura , Estimulación Luminosa , Células Fotorreceptoras de Invertebrados/químicaRESUMEN
Many neurons use graded membrane-potential changes, instead of action potentials, to transmit information. Traditional synaptic models feature discontinuous transmitter release by presynaptic action potentials, but this is not true for synapses between graded-potential neurons. In addition to graded and continuous transmitter release, they have multiple active zones, ribbon formations and L-type Ca2+ channels. These differences are probably linked to the high rate of vesicle fusion required for continuous transmitter release. Early stages of sensory systems provide some of the best characterized graded-potential neurons, and recent work on these systems suggests that modification of synaptic transmission by adaptation is a powerful feature of graded synapses.
Asunto(s)
Neuronas/fisiología , Sinapsis/fisiología , Transmisión Sináptica/fisiología , Animales , Neuronas/ultraestructuraRESUMEN
1. Randomly modulated light stimuli were used to characterize the nonlinear dynamic properties of the synapse between photoreceptors and large monopolar neurons (LMC) in the fly retina. Membrane potential fluctuations produced by constant variance contrast stimuli were recorded at eight different levels of background light intensity. 2. Representation of the photoreceptor-LMC input-output data in the form of traditional characteristic curves indicated that synaptic gain was reduced by light adaptation. However, this representation did not include the time-dependent properties of the synaptic function, which are known to be nonlinear. Therefore nonlinear systems analysis was used to characterize the synapse. 3. The responses of photoreceptors and LMCs to random light fluctuations were characterized by second-order Volterra series, with kernel estimation by the parallel cascade method. Photoreceptor responses were approximately linear, but LMC responses were clearly nonlinear. 4. Synaptic input-output relationships were measured by passing the light stimuli to LMCs through the measured photoreceptor characteristics to obtain an estimate of the synaptic input. The resulting nonlinear synaptic functions were well characterized by second-order Volterra series. They could not be modeled by a linear-nonlinear-linear cascade but were better approximated by a nonlinear-linear-nonlinear cascade. 5. These results support two possible structural models of the synapse, the first having two parallel paths for signal flow between the photoreceptor and LMC, and the second having two distinct nonlinear operations, occurring before and after chemical transmission. 6. The two models were cach used to calculate the synaptic gain to a brief change in photoreceptor membrane potential. Both models predicted that synaptic gain is reduced by light adaptation.
Asunto(s)
Adaptación Ocular/fisiología , Dípteros/fisiología , Retina/fisiología , Sinapsis/fisiología , Algoritmos , Animales , Potenciales de la Membrana/fisiología , Modelos Biológicos , Neuronas Aferentes/fisiología , Dinámicas no Lineales , Estimulación Luminosa , Células Fotorreceptoras de Invertebrados/fisiología , Transmisión Sináptica/fisiologíaRESUMEN
1. We studied graded synaptic transmission in the fly photoreceptor-interneuron synapse by using intracellular in situ recordings from pre- and postsynaptic cells. 2. A large presynaptic hyperpolarization after light adaptation, caused by the activation of the electrogenic Na+/K+ pump, drastically reduced the conspicuous postsynaptic dark noise. At the same time, the postsynaptic neurons depolarized, with an increase of input resistance of 5-10 M omega. 3. The spectral characteristics of the postsynaptic membrane noise in dark and during noise reduction, together with the other results, suggested that the transmitter release decreased dramatically approximately 12 mV below the resting potential of the presynaptic photoreceptors. 4. During the postsynaptic noise reduction, the saturated and subsaturated first-order visual interneuron responses were increased up to 9 mV with a time constant of recovery of approximately 10 s. This increase was shown to be caused by the negative shift of the reversal potential of the transmitter-gated (mainly Cl-) conductance, caused apparently by the reduced transmitter input. 5. The results strongly suggest that the photoreceptor transmitter release in fly is tonic, even in dark, and further support the modulation of the synaptic voltage transfer by postsynaptic Cl- extrusion.
Asunto(s)
Dípteros/fisiología , Neurotransmisores/metabolismo , Sinapsis/metabolismo , Animales , Canales de Cloruro/metabolismo , Electrofisiología , Técnicas In Vitro , Interneuronas/metabolismo , Activación del Canal Iónico/fisiología , Células Fotorreceptoras de Invertebrados/fisiología , Receptores Presinapticos/fisiología , ATPasa Intercambiadora de Sodio-Potasio/fisiologíaRESUMEN
1. We studied the graded and spiking properties of the "non-spiking" first-order visual interneurons of the fly compound eye in situ with the use of intracellular recordings. Iontophoretical QX-314 injections, Lucifer yellow marking, and (discontinuous) current-clamp method together with transfer function analysis were used to characterize the neural signal processing mechanisms in these neurons. 2. A light-OFF spike was seen in one identified anatomic subtype (L3, n = 6) of the three first-order visual interneurons (L1, L2, and L3, or LMCs) when recorded from synaptic region (i.e., in the 1st visual ganglion, lamina ganglionaris) in dark-adapted conditions. Hyperpolarization of the membrane potential by current caused the identified L1 (n = 4), as well as L3 (n = 6), to produce an OFF spike, a number of action potentials, and some subthreshold depolarizations after the light-ON response. In L2 the OFF spike or action potentials could not be elicited. 3. To produce action potentials in L1 and L3, it was found to be necessary to hyperpolarize the cells approximately 35-45 mV (n = 43) below the resting potential (RP) in the synaptic zone. Recordings from the axons of these cells revealed that near the second neuropil (chiasma) the threshold of these spikes was near to (approximately 10 mV below, n = 16) or even at the RP when an ON spike was also produced (n = 4). 4. The recorded spikes were up to 54 mV in amplitude, appeared with a maximum frequency of up to 120 impulses/s, and had a duration of approximately 8 ms. In L1 and L3 the spikes were elicited either after a light pulse (L3) or after a negative current step that was superimposed on a hyperpolarizing steady-state current (L3 and L1). A positive current step (similarly superimposed on a hyperpolarizing steady-state current) also triggered the spikes during the step. 5. Iontophoretic injection of a potent intracellularly effective blocker of voltage-gated sodium channels, QX-314, irreversibly eradicated the spikes and subthreshold depolarizations (n = 5). In addition, further injections elongated the light-ON responses and decreased or even abolished the light-OFF response. 6. Negative prepulses followed by positive current steps were applied from the RP, to test the activation-inactivation properties of the channels responsible for the OFF spike.(ABSTRACT TRUNCATED AT 400 WORDS)
Asunto(s)
Dípteros/fisiología , Interneuronas/fisiología , Fenómenos Fisiológicos Oculares , Canales de Sodio/fisiología , Potenciales de Acción/fisiología , Anestésicos Locales/farmacología , Animales , Axones/fisiología , Adaptación a la Oscuridad/fisiología , Iontoforesis , Lidocaína/análogos & derivados , Lidocaína/farmacología , Luz , Células Fotorreceptoras de Invertebrados/fisiología , Retina/fisiologíaRESUMEN
To characterize the transfer of graded potentials and the properties of the associated noise in the photoreceptor-interneuron synapse of the blowfly (Calliphora vicina) compound eye, we recorded voltage responses of photoreceptors (R1-6) and large monopolar cells (LMC) evoked by: (a) steps of light presented in the dark; (b) contrast steps; and (c) pseudorandomly modulated contrast stimuli at backgrounds covering 6 log intensity units. Additionally, we made recordings from photoreceptor axon terminals. Increased light adaptation gradually changed the synaptic signal transfer from low-pass to band-pass filtering. This was accompanied by decreased synaptic delay and increased contrast gain, but the overall synaptic gain and the intrinsic noise (i.e., transmission noise) were reduced. Based on these results, we describe a descriptive synaptic model, in which the kinetics of the tonic transmitter (histamine) release from the photoreceptor axon terminals change with mean photoreceptor depolarization. During signal transmission, tonic transmitter release is augmented by voltage-dependent contrast-enhancing mechanisms in the photoreceptor axons that produce fast transients from the rising phases of the photoreceptor responses and add these enhanced voltages to the original photoreceptor responses. The model can predict the experimental findings and it agrees with the recently proposed theory of maximizing sensory information.
Asunto(s)
Dípteros/fisiología , Interneuronas/fisiología , Células Fotorreceptoras de Invertebrados/fisiología , Sinapsis/fisiología , Animales , Adaptación a la Oscuridad/fisiología , Electrofisiología , Liberación de Histamina/fisiología , Interneuronas/metabolismo , Potenciales de la Membrana/fisiología , Neurotransmisores/metabolismo , Fenómenos Fisiológicos Oculares , Estimulación Luminosa , Células Fotorreceptoras de Invertebrados/metabolismo , Terminales Presinápticos/fisiología , Sinapsis/metabolismoRESUMEN
Light-adapted fly photoreceptor cells were stimulated with brief positive and negative contrast flashes (contrast = delta I/I, I = intensity). Membrane potential responses to a wide range of flash intensities were well-fitted by a static nonlinearity followed by a compartmental model represented by a gamma function. However, the agreement improved if one parameter of the gamma function, n, varied quadratically with input light intensity. Response amplitude and time to peak were estimated from the fitted parameters. Response amplitude varied approximately linearly with contrast but showed nonlinear compression with the largest negative flashes. Reducing the background light level by 3 decades or hyperpolarizing the cell electrically produced stronger nonlinear compression with both contrast polarities. This is probably due to fast voltage-activated K+ channels. Responses to double flashes with varying time separations were well-fitted by summed gamma functions, allowing separation of the individual flash responses. There was no detectable time-dependent interaction between paired positive flashes at all separations. However, the response to two negative flashes was greater than the linear prediction at short separations, and this facilitatory nonlinearity decayed with a time constant of about 1 msec. The facilitation is probably related to resonant behavior in light-adapted photoreceptors and may be due to an IP3-induced intracellular Ca2+ release.
Asunto(s)
Adaptación a la Oscuridad/fisiología , Dípteros/fisiología , Células Fotorreceptoras de Invertebrados/fisiología , Animales , ATPasas Transportadoras de Calcio , Estudios de Evaluación como Asunto , Modelos Lineales , Potenciales de la Membrana , Modelos Biológicos , Modelos Estadísticos , Tiempo de Reacción , Factores de TiempoRESUMEN
1. We have used intracellular recordings and ionophoretic injections in vivo to investigate the ion exchange mechanisms responsible for the maintenance of the ion gradients in the large monopolar cells (LMCs) of the first optic ganglion of the blowfly, Calliphora vicinia. 2. Ionophoretic chloride injections caused a rapid approximately 20-mV depolarization of the resting potential (Erp) and abolished or even reversed the light-ON response (OR), which is caused by histamine-gated chloride conductance, as the chloride equilibrium potential (ECl) was increased beyond the Erp, i.e., 50 mV upward. Ionophoretic sodium injections were found to mimic the action of the ionophoretic chloride injections and thus also to cause chloride accumulation inside the cell. 3. Ionophoretic injections of bicarbonate only had the effect of hyperpolarizing the Erp by 5-15 mV for 1-25 s, but chloride gradient, i.e., ECl remained unchanged. Intracellular proton load caused depolarization of the Erp by 15 +/- 5 mV (mean +/- SE) for 20-25 s and a slight 15 +/- 5-mV decrease of the peak OR. Ionophoretic injections of potassium, acetate, and furosemide failed to cause any physiological effect. 4. The time constant for the recovery of the peak OR after sodium load increased linearly as a function of injected charge whereby the time constant for the recovery after chloride accumulation increased slowly up to 50 nC of injected charge, after which it increased rapidly, possibly indicating substrate inhibition. The time constant for the recovery of peak OR after sodium load was from 5 to 65 nC greater than that of chloride.(ABSTRACT TRUNCATED AT 250 WORDS)