Timing and Balance of Inhibition Enhance the Effect of Long-Term Potentiation on Cell Firing

Marder, Carrie P.; Buonomano, Dean V.

doi:10.1523/jneurosci.2661-04.2004

Cited by 52 publications

(61 citation statements)

References 70 publications

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“…In our study, PS LTP was depressed whereas EPSP LTP was not in the morphine group, suggesting that prenatal morphine exposure impaired EPSP-spike potentiation. EPSP-spike potentiation depends on the balance and timing of GABA A ergic inhibition (Marder and Buonomano, 2004). GABA A R antagonists such as picrotoxin or bicuculline could block the EPSP-spike potentiation (Abraham et al, 1987;Lu et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

“…We also evaluated spatial memory in these offspring using a two-trial Y-maze test (Dellu et al, 1997), since the DG area of the hippocampus has been associated with spatial memory (Colicos and Dash, 1996;Nilsson et al, 1999;Rubin et al, 1999). Finally we determined whether GABA-containing neurons in the DG area, which largely control the EPSP/spike relationship (Tomasulo et al, 1991;Marder and Buonomano, 2004) and the functions of dentate granule cells (Coulter and Carlson, 2007), would be alternated by prenatal morphine exposure. These studies suggest that prenatal morphine exposure decreased in vivo synaptic plasticity and the number of GABA-containing neurons in the DG area of juvenile rat offspring with deficient spatial memory.…”

Section: Introductionmentioning

confidence: 99%

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Impaired in vivo synaptic plasticity in dentate gyrus and spatial memory in juvenile rats induced by prenatal morphine exposure

et al. 2008

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ABSTRACT:Prenatal morphine exposure induces neurobiological changes, including deficits in learning and memory, in juvenile rat offspring. However the effects of this exposure on hippocampal plasticity, which is critical for learning and memory processes, are not well understood. The present study investigates the alterations of spatial memory and in vivo hippocampal synaptic plasticity in juvenile rats prenatally exposed to morphine. On gestation days 11-18, pregnant rats were randomly chosen to be injected twice daily with morphine or saline. Each juvenile offspring (postnatal day 22-31) performed one two-trial Y-maze task to evaluate spatial memory. Afterwards, the in vivo field excitatory postsynaptic potential (fEPSP) and population spike (PS) were recorded in the perforant path dentate gyrus (DG) pathway in the hippocampus. Prenatal morphine exposure reduced depotentiation (DP), but not longterm potentiation (LTP), of the EPSP slope. However, both LTP and DP of the EPSP slope were depressed in prenatal morphine-exposed juvenile offspring. The morphine group also showed poorer performance for the Y-maze task than the control group. Depressed PS LTP, but not EPSP LTP, in the morphine group suggested that prenatal morphine exposure changed GABAergic inhibition, which mediates EPSP-spike potentiation. Then a loss of GABA-containing neurons in the DG area of the morphine group was observed using immunohistochemistry. Taken together, our results suggest that prenatal morphine exposure impairs the juvenile offspring's dentate synaptic plasticity and spatial memory, and that decreased GABAergic inhibition may play a role in these effects. These findings might contribute to an explanation for the cognitive deficits in children whose mothers abuse opiates during pregnancy. V V C 2008 WileyLiss, Inc.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Impaired in vivo synaptic plasticity in dentate gyrus and spatial memory in juvenile rats induced by prenatal morphine exposure

et al. 2008

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“…In nature, the laminated inputs may be active simultaneously and are modulated by dendritic, somatic, and axonal inhibition. In particular, inhibition may play a major role in the input-output function of pyramidal cells (Marder and Buonomano, 2004). Moreover, the gradient of GABA B to GABA A currents in these cells (Pettit and Augustine, 2000) could differentially affect synaptic integration in distal vs. proximal inputs.…”

Section: Discussionmentioning

confidence: 99%

Computational simulation of the input-output relationship in hippocampal pyramidal cells

Ascoli

2006

J Comput Neurosci

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The precise mapping of how complex patterns of synaptic inputs are integrated into specific patterns of spiking output is an essential step in the characterization of the cellular basis of network dynamics and function. Relative to other principal neurons of the hippocampus, the electrophysiology of CA1 pyramidal cells has been extensively investigated. Yet, the precise input-output relationship is to date unknown even for this neuronal class. CA1 pyramidal neurons receive laminated excitatory inputs from three distinct pathways: recurrent CA1 collaterals on basal dendrites, CA3 Schaffer collaterals, mostly on oblique and proximal apical dendrites, and entorhinal perforant pathway on distal apical dendrites. We implemented detailed computer simulations of pyramidal cell electrophysiology based on three-dimensional anatomical reconstructions and compartmental models of available biophysical properties from the experimental literature. To investigate the effect of synaptic input on axosomatic firing, we stochastically distributed a realistic number of excitatory synapses in each of the three dendritic layers. We then recorded the spiking response to different stimulation patterns. For all dendritic layers, synchronous stimuli resulted in trains of spiking output and a linear relationship between input and output firing frequencies. In contrast, asynchronous stimuli evoked non-bursting spike patterns and the corresponding firing frequency input-output function was logarithmic. The regular/irregular nature of the input synaptic intervals was only reflected in the regularity of output inter-burst intervals in response to synchronous stimulation, and never affected firing frequency. Synaptic stimulations in the basal and proximal apical trees across individual neuronal morphologies yielded remarkably similar input-output relationships. Results were also robust with respect to the detailed distributions of dendritic and synaptic conductances within a plausible range constrained by experimental evidence. In contrast, the input-output relationship in response to distal apical stimuli showed dramatic differences from the other dendritic locations as well as among neurons, and was more sensible to the exact channel densities.

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“…DZ decreases the CV for responses to 20 cd/m 2 luminance compared with controls but not for other luminances tested, suggesting increased I/E can improve temporal fidelity of responses for some stimuli. The synaptic I/E ratio has been shown to affect the latency to fire action potentials (Carvalho and Buonomano 2009;Marder and Buonomano 2004;Tiesinga et al 2008). First spike Decreasing I/E increased the distribution of first spike latencies for stimuli of 10 cd/m 2 , whereas increasing I/E narrowed the distribution of first spike latencies for stimuli of 20 cd/m 2 .…”

Section: Knockdown Of the ␥2 Subunit Of Gaba A Rmentioning

confidence: 99%

Inhibition to excitation ratio regulates visual system responses and behavior in vivo

Shen

McKeown

Demas

et al. 2011

Journal of Neurophysiology

106

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The balance of inhibitory to excitatory (I/E) synaptic inputs is thought to control information processing and behavioral output of the central nervous system. We sought to test the effects of the decreased or increased I/E ratio on visual circuit function and visually guided behavior in Xenopus tadpoles. We selectively decreased inhibitory synaptic transmission in optic tectal neurons by knocking down the γ2 subunit of the GABA(A) receptors (GABA(A)R) using antisense morpholino oligonucleotides or by expressing a peptide corresponding to an intracellular loop of the γ2 subunit, called ICL, which interferes with anchoring GABA(A)R at synapses. Recordings of miniature inhibitory postsynaptic currents (mIPSCs) and miniature excitatory PSCs (mEPSCs) showed that these treatments decreased the frequency of mIPSCs compared with control tectal neurons without affecting mEPSC frequency, resulting in an ∼50% decrease in the ratio of I/E synaptic input. ICL expression and γ2-subunit knockdown also decreased the ratio of optic nerve-evoked synaptic I/E responses. We recorded visually evoked responses from optic tectal neurons, in which the synaptic I/E ratio was decreased. Decreasing the synaptic I/E ratio in tectal neurons increased the variance of first spike latency in response to full-field visual stimulation, increased recurrent activity in the tectal circuit, enlarged spatial receptive fields, and lengthened the temporal integration window. We used the benzodiazepine, diazepam (DZ), to increase inhibitory synaptic activity. DZ increased optic nerve-evoked inhibitory transmission but did not affect evoked excitatory currents, resulting in an increase in the I/E ratio of ∼30%. Increasing the I/E ratio with DZ decreased the variance of first spike latency, decreased spatial receptive field size, and lengthened temporal receptive fields. Sequential recordings of spikes and excitatory and inhibitory synaptic inputs to the same visual stimuli demonstrated that decreasing or increasing the I/E ratio disrupted input/output relations. We assessed the effect of an altered I/E ratio on a visually guided behavior that requires the optic tectum. Increasing and decreasing I/E in tectal neurons blocked the tectally mediated visual avoidance behavior. Because ICL expression, γ2-subunit knockdown, and DZ did not directly affect excitatory synaptic transmission, we interpret the results of our study as evidence that partially decreasing or increasing the ratio of I/E disrupts several measures of visual system information processing and visually guided behavior in an intact vertebrate.

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Timing and Balance of Inhibition Enhance the Effect of Long-Term Potentiation on Cell Firing

Cited by 52 publications

References 70 publications

Impaired in vivo synaptic plasticity in dentate gyrus and spatial memory in juvenile rats induced by prenatal morphine exposure

Impaired in vivo synaptic plasticity in dentate gyrus and spatial memory in juvenile rats induced by prenatal morphine exposure

Computational simulation of the input-output relationship in hippocampal pyramidal cells

Inhibition to excitation ratio regulates visual system responses and behavior in vivo

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