Synaptic Dynamics on Different Time Scales in a Parallel Fiber Feedback Pathway of the Weakly Electric Fish

2004 ◽  
Vol 91 (2) ◽  
pp. 1064-1070 ◽  
Author(s):  
John E. Lewis ◽  
Leonard Maler
Keyword(s):  
Time Scales ◽  
Electric Fish ◽  
Parallel Fiber ◽  
Weakly Electric Fish ◽  
Short Term ◽  
Parallel Fibers ◽  
Short Term Plasticity ◽  
Synaptic Dynamics ◽  
Weakly Electric

Synaptic dynamics comprise a variety of interacting processes acting on a wide range of time scales. This enables a synapse to perform a large array of computations, from temporal and spatial filtering to associative learning. In this study, we describe how changing synaptic gain via long-term plasticity can act to shape the temporal filtering of a synapse through modulation of short-term plasticity. In the weakly electric fish, parallel fibers from cerebellar granule cells provide massive feedback inputs to the pyramidal neurons of the electrosensory lateral line lobe. We demonstrate a long-term synaptic enhancement (LTE) of these synapses that is biochemically similar to the presynaptic long-term potentiation expressed by parallel fibers in the mammalian cerebellum. Using a novel stimulation protocol and a simple modeling paradigm, we then quantify the changes in short-term plasticity during the induction of LTE and show that these changes can be explained by gradual changes in only one model parameter, that which is associated with the baseline probability of transmitter release. These changes lead to a shift in the spike frequency preference of the synapse, suggesting that long-term plasticity is not only involved in controlling the gain of the parallel fiber synapse, but also provides a means of controlling synaptic filtering over multiple time scales.

Global Electrosensory Oscillations Enhance Directional Responses of Midbrain Neurons in Eigenmannia

2006 ◽  
Vol 96 (5) ◽  
pp. 2319-2326 ◽  
Author(s):  
J. U. Ramcharitar ◽  
E. W. Tan ◽  
E. S. Fortune
Keyword(s):  
Electric Fish ◽  
Moving Objects ◽  
Synaptic Depression ◽  
Weakly Electric Fish ◽  
Directional Selectivity ◽  
Short Term ◽  
Midbrain Neurons ◽  
Transmission Of Information ◽  
Jamming Avoidance ◽  
Weakly Electric

Eigenmannia, a genus of weakly electric fish, exhibits a specialized behavior known as the jamming avoidance response (JAR). The JAR results in a categorical difference between Eigenmannia that are in groups of conspecifics and those that are alone. Fish in groups exhibit the JAR behavior and thereby experience ongoing, global synchronous 20- to 50-Hz electrosensory oscillations, whereas solitary fish do not. Although previous work has shown that these ongoing signals do not significantly degrade electrosensory behavior, these oscillations nevertheless elicit short-term synaptic depression in midbrain circuits. Because short-term synaptic depression can have profound effects on the transmission of information through synapses, we examined the differences in intracellularly recorded responses of midbrain neurons in awake, behaving fish to moving electrosensory images under electrosensory conditions that mimic solitary fish and fish in groups. In solitary conditions, moving objects elicited Gaussian or sinusoidal postsynaptic potentials (PSPs) that commonly exhibited preferential responses to a direction of motion. Surprisingly, when the same stimulus was presented in the presence of the global oscillations, directional selectivity was increased in all neurons tested. The magnitudes of the differences in PSP amplitude for preferred and nonpreferred directions were correlated with a measure of short-term synaptic depression in both conditions. The electrosensory consequences of the JAR appear to result in an enhancement of the representation of direction of motion in midbrain neurons. The data also support a role for short-term synaptic depression in the generation and modulation of directional responses.

Dynamics of Electrosensory Feedback: Short-Term Plasticity and Inhibition in a Parallel Fiber Pathway

2002 ◽  
Vol 88 (4) ◽  
pp. 1695-1706 ◽  
Author(s):  
John E. Lewis ◽  
Leonard Maler
Keyword(s):  
Pyramidal Neurons ◽  
Molecular Layer ◽  
Parallel Fiber ◽  
Weakly Electric Fish ◽  
Short Term ◽  
Stimulus Interval ◽  
Simple Description ◽  
Feed Forward ◽  
Synaptic Dynamics ◽  
Feed Forward Inhibition

The dynamics of neuronal feedback pathways are generally not well understood. This is due to the complexity arising from the combined dynamics of closed-loop feedback systems and the synaptic plasticity of feedback connections. Here, we investigate the short-term synaptic dynamics underlying the parallel fiber feedback pathway to a primary electrosensory nucleus in the weakly electric fish, Apteronotus leptorhynchus. In open-loop conditions, the dynamics of this pathway arise from a monosynaptic excitatory connection and a disynaptic (feed-forward) inhibitory connection to pyramidal neurons in the electrosensory lateral line lobe (ELL). In a brain slice preparation of the ELL, we characterized the synaptic responses of pyramidal neurons to short trains of electrical stimuli delivered to the parallel fibers of the dorsal molecular layer. Stimulus trains consisted of 20 pulses, at either random intervals or constant intervals, with varying mean frequencies. With random trains, pyramidal neuron responses were well described by a single exponential function of the inter-stimulus interval—suggesting a single facilitation-like process underlies these synaptic dynamics. However, responses to periodic (constant interval) trains deviated from this simple description. Random and periodic stimulus trains delivered when the feed-forward inhibitory component of this pathway was pharmacologically blocked revealed that inhibition and depression also contribute to the observed dynamics. We formulated a simple model of the parallel fiber synaptic dynamics that provided an accurate description of our data. The model dynamics resulted from a combination of three distinct processes. Two of the processes are the classically-described synaptic facilitation and depression, and the third is a novel description of feed-forward inhibition. An analysis of this model suggests that synaptic pathways combining plasticity with feed-forward inhibition can be easily tuned to signal different types of transient stimuli and thus lead to diverse and nonintuitive filtering properties.

scholarly journals Presynaptic CB1 Receptors Regulate Synaptic Plasticity at Cerebellar Parallel Fiber Synapses

2011 ◽  
Vol 105 (2) ◽  
pp. 958-963 ◽  
Author(s):  
Megan R. Carey ◽  
Michael H. Myoga ◽  
Kimberly R. McDaniels ◽  
Giovanni Marsicano ◽  
Beat Lutz ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Purkinje Cells ◽  
Cannabinoid Receptors ◽  
Granule Cells ◽  
Cerebellar Granule Cells ◽  
Inhibitory Interneuron ◽  
Parallel Fiber ◽  
Short Term ◽  
Short Term Plasticity

Endocannabinoids are potent regulators of synaptic strength. They are generally thought to modify neurotransmitter release through retrograde activation of presynaptic type 1 cannabinoid receptors (CB1Rs). In the cerebellar cortex, CB1Rs regulate several forms of synaptic plasticity at synapses onto Purkinje cells, including presynaptically expressed short-term plasticity and, somewhat paradoxically, a postsynaptic form of long-term depression (LTD). Here we have generated mice in which CB1Rs were selectively eliminated from cerebellar granule cells, whose axons form parallel fibers. We find that in these mice, endocannabinoid-dependent short-term plasticity is eliminated at parallel fiber, but not inhibitory interneuron, synapses onto Purkinje cells. Further, parallel fiber LTD is not observed in these mice, indicating that presynaptic CB1Rs regulate long-term plasticity at this synapse.

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