Spatial integration of local transmitter responses in motoneurones of the turtle spinal cord in vitro.

Skydsgaard, Mikala; Hounsgaard, Jørn

doi:10.1113/jphysiol.1994.sp020291

Cited by 39 publications

(35 citation statements)

References 34 publications

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“…In turtle spinal motoneurons, Ca 2+ conductances are present in dendrites (522), which may have important consequences for the transfer of synaptic input (1162), and in the generation and modulation of plateau potentials (521,522,524,1200). In rat spinal motoneurons, L-type Ca 2+ channels are present in the somatic and proximal dendritic membrane and N-type Ca 2+ channels in both the dendritic and somatic membrane (1351).…”

Section: Active Membrane Properties Of Motoneuronsmentioning

confidence: 99%

“…However, a conductance increase during the depolarized, relative to hyperpolarized, phase of the locomotor cycle occurs in only 8% of motoneurons (1139). Lack of phasic oscillation in input conductance in association with glutamatergic-mediated depolarization may reflect arrival of locomotor inputs on distal synapses where conductance changes are not detected with somatic intracellular recording (1162). Also, inhibitory inputs during the hyperpolarized phase of the cycle may produce increases in conductance similar to those produced during the depolarized phase by the excitatory inputs.…”

Section: A) Presynaptic Actionsmentioning

confidence: 99%

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Synaptic Control of Motoneuronal Excitability

Rekling

Funk

Bayliss

et al. 2000

Physiological Reviews

537

482

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Movement, the fundamental component of behavior and the principal extrinsic action of the brain, is produced when skeletal muscles contract and relax in response to patterns of action potentials generated by motoneurons. The processes that determine the firing behavior of motoneurons are therefore important in understanding the transformation of neural activity to motor behavior. Here, we review recent studies on the control of motoneuronal excitability, focusing on synaptic and cellular properties. We first present a background description of motoneurons: their development, anatomical organization, and membrane properties, both passive and active. We then describe the general anatomical organization of synaptic input to motoneurons, followed by a description of the major transmitter systems that affect motoneuronal excitability, including ligands, receptor distribution, pre-and postsynaptic actions, signal transduction, and functional role. Glutamate is the main excitatory, and GABA and glycine are the main inhibitory transmitters acting through ionotropic receptors. These amino acids signal the principal motor commands from peripheral, spinal, and supraspinal structures. Amines, such as serotonin and norepinephrine, and neuropeptides, as well as the glutamate and GABA acting at metabotropic receptors, modulate motoneuronal excitability through pre-and postsynaptic actions. Acting principally via second messenger systems, their actions converge on common effectors, e.g., leak K + current, cationic inward current, hyperpolarization-activated inward current, Ca 2+ channels, or presynaptic release processes. Together, these numerous inputs mediate and modify incoming motor commands, ultimately generating the coordinated firing patterns that underlie muscle contractions during motor behavior.

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Section: Active Membrane Properties Of Motoneuronsmentioning

confidence: 99%

Section: A) Presynaptic Actionsmentioning

confidence: 99%

Synaptic Control of Motoneuronal Excitability

Rekling

Funk

Bayliss

et al. 2000

Physiological Reviews

537

482

View full text Add to dashboard Cite

show abstract

“…Electrophysiological analysis in vivo showed sublinear summation in motoneurons (Kuno and Miyahara, 1969) and both linear and nonlinear modes of integration of responses in the visual system (Douglas et al, 1988;Jagadeesh et al, 1993Jagadeesh et al, , 1997Borggraham et al, 1998;Hirsch et al, 1998;Kogo and Ariel, 1999;Anderson et al, 2000). Experiments in brain slices indicated linear input summation in motoneurons (Skydsgaard and Hounsgaard, 1994) and hippocampal pyramidal cells (Langmoen and Andersen, 1983). Physiological tests without the additional information on the subcellular position of inputs leave dendritic integration rules open to several interpretations (Major et al, 1994; Z ador et al, 1995;Mainen et al, 1996).…”

Section: Abstract: Cerebral Cortex; Integration; Ipsp; Epsp; Internementioning

confidence: 99%

Cell Type- and Subcellular Position-Dependent Summation of Unitary Postsynaptic Potentials in Neocortical Neurons

2002

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Theoretical studies predict that the modes of integration of coincident inputs depend on their location and timing. To test these models experimentally, we simultaneously recorded from three neocortical neurons in vitro and investigated the effect of the subcellular position of two convergent inputs on the response summation in the common postsynaptic cell. When scattered over the somatodendritic surface, combination of two coincident excitatory or inhibitory synaptic potentials summed linearly in layer 2/3 pyramidal cells, as well as in GABAergic interneurons. Slightly sublinear summation with connection specific kinetics was observed when convergent inputs targeted closely placed sites on the postsynaptic cell. The degree of linearity of summation also depended on the type of connection, the relative timing of inputs, and the activation state of I h . The results suggest that, when few inputs are active, the majority of afferent permutations undergo linear integration, maintaining the importance of individual inputs. However, compartment-and connection-specific nonlinear interactions between synapses located close to each other could increase the computational power of individual neurons in a cell typespecific manner. Key words: cerebral cortex; integration; IPSP; EPSP; interneuron; pyramidal cellThe rules of synaptic summation are thought to depend on the dendritic geometry of the postsynaptic cell (Zador et al., 1995;Mainen et al., 1996), on a variety of synaptic-and voltagedependent conductances distributed heterogeneously over the dendritic tree (Johnston et al., 1996;Hausser et al., 2000), and on the relative position and timing of inputs (Jack et al., 1975;Shepherd and Brayton, 1987;Rall et al., 1992;Segev et al., 1995;Hausser et al., 2000). Theoretical analysis of dendritic integration began by assuming that passive cables serve as reasonable models of dendrites (Jack et al., 1975;Segev et al., 1995). According to cable theory, electrically isolated inputs sum linearly, whereas closely located inputs produce an attenuated response as a consequence of reduction in the ionic driving force or a decrease in dendritic input resistance leading to shunting of synaptic currents (Jack et al., 1975;Segev et al., 1995). However, dendritic membranes are not passive, because they contain voltage-dependent conductances, which could selectively amplify distal inputs or subserve local nonlinear operations (Koch et al., 1983;Mel, 1993). Direct experimental determination of the influence of the location of synaptic inputs on dendritic integration has been relatively sparse. Electrophysiological analysis in vivo showed sublinear summation in motoneurons (Kuno and Miyahara, 1969) and both linear and nonlinear modes of integration of responses in the visual system (Douglas et al., 1988;Jagadeesh et al., 1993Jagadeesh et al., , 1997Borggraham et al., 1998;Hirsch et al., 1998;Kogo and Ariel, 1999;Anderson et al., 2000). Experiments in brain slices indicated linear input summation in motoneurons (Skydsgaard and Hounsgaard, 199...

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“…All of the experimental data lead to the conclusion that nonlinear summation of synaptic inputs to motoneurons is negligible or, at the most, modest (Burke 1967;Burke et al 1971;Clements at al. 1986;Kuno and Miyahara 1969;Powers and Binder 2000;Rall et al 1967;Skydsgaard and Hounsgaard 1994;however, see Curtis and Eccles 1959). For example, near the threshold for repetitive firing, the current reaching the soma generated by combined activation of pairs of inputs (e.g., Ia afferents and axons from Dieters nucleus) was, on average, within 7% of the linear sum of the currents generated by each input (Powers and Binder 2000).…”

Section: Introductionmentioning

confidence: 99%

Effect of Nonlinear Summation of Synaptic Currents on the Input–Output Properties of Spinal Motoneurons

Cushing¹,

Bui²,

Rose³

2005

Journal of Neurophysiology

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Cushing, S., T. Bui, and P. K. Rose. Effect of nonlinear summation of synaptic currents on the input-output properties of spinal motoneurons. J Neurophysiol 94: 3465-3478, 2005. First published August 3, 2005 doi:10.1152/jn.00439.2005. A single spinal motoneuron receives tens of thousands of synapses. The neurotransmitters released by many of these synapses act on iontotropic receptors and alter the driving potential of neighboring synapses. This interaction introduces an intrinsic nonlinearity in motoneuron input-output properties where the response to two simultaneous inputs is less than the linear sum of the responses to each input alone. Our goal was to determine the impact of this nonlinearity on the current delivered to the soma during activation of predetermined numbers and distributions of excitatory and inhibitory synapses. To accomplish this goal we constructed compartmental models constrained by detailed measurements of the geometry of the dendritic trees of three feline motoneurons. The current "lost" as a result of local changes in driving potential was substantial and resulted in a highly nonlinear relationship between the number of active synapses and the current reaching the soma. Background synaptic activity consisting of a balanced activation of excitatory and inhibitory synapses further decreased the current delivered to the soma, but reduced the nonlinearity with respect to the total number of active excitatory synapses. Unexpectedly, simulations that mimicked experimental measures of nonlinear summation, activation of two sets of excitatory synapses, resulted in nearly linear summation. This result suggests that nonlinear summation can be difficult to detect, despite the substantial "loss" of current arising from nonlinear summation. The magnitude of this "loss" appears to limit motoneuron activity, based solely on activation of iontotropic receptors, to levels that are inadequate to generate functionally meaningful muscle forces.

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Spatial integration of local transmitter responses in motoneurones of the turtle spinal cord in vitro.

Cited by 39 publications

References 34 publications

Synaptic Control of Motoneuronal Excitability

Synaptic Control of Motoneuronal Excitability

Cell Type- and Subcellular Position-Dependent Summation of Unitary Postsynaptic Potentials in Neocortical Neurons

Effect of Nonlinear Summation of Synaptic Currents on the Input–Output Properties of Spinal Motoneurons

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