Activity-dependent reconfiguration of the effective dendritic field of motoneurons

Abducens neurons undergo a dose-dependent synaptic blockade (either disinhibition or complete blockade) when tetanus neurotoxin (TeNT) is injected into the lateral rectus muscle at either a low (0.5) or a high dose (5 ng/kg). We studied the firing pattern and recruitment order in abducens neurons both in control and after TeNT injection. The eye position threshold for recruitment of control abducens neurons was exponentially related to the eye position and velocity sensitivities. We also found a constancy of recruitment threshold for different eye movement modalities (spontaneous, optokinetic, and vestibular). Exponential relationships were found, as well, for eye velocity sensitivity during saccades and for position and velocity sensitivities during the vestibulo-ocular reflex. Likewise, inverse relationships were found between recruitment threshold or position sensitivity with the antidromic latency in control abducens neurons. These relationships, however, did not apply following TeNT treatment. Neuronal firing after TeNT appeared either disinhibited (low dose) or depressed (high dose), but the relationships between neuronal sensitivities and recruitment still applied. However, the pattern of recruitment shifted toward the treated side as more inputs were blocked by the low-and high-dose treatments, respectively. Nonetheless, although the recruitment-to-sensitivity relationships persisted under the TeNT synaptic blockade, we conclude that synaptic inputs are determinant for establishing the recruitment threshold and recruitment spacing of abducens motoneurons and internuclear neurons.

Section: Intrinsic Correlates To Recruitment Ordermentioning

confidence: 99%

Recruitment Order of Cat Abducens Motoneurons and Internuclear Neurons

Pastor

González-Forero

2003

“…In contrast, predictions based on cable theory (i.e., analytically tractable models of neurons with arbitrary geometry, innervation patterns, and synaptic conductances) conclude that interactions between neighboring synapses resulting from changes in synaptic driving potential could profoundly reduce the summation of postsynaptic potentials (Holmes and Woody 1989;Jack et al 1975;Koch 1999;MacGregor 1968;Rall 1964Rall 1967Segev and Parnas 1983;Spruston et al 1999) and the amplitude of the synaptic current reaching the soma (Abbott 1991;Koch 1999). These conclusions have been reinforced by simulations that incorporate more realistic descriptions of motoneuron geometry, synaptic density, magnitude, and time course of synaptic conductances (Barrett 1975;Barrett and Crill 1974b;Binder et al 1996;Korogod et al 2000;Powers and Binder 2001;Ulrich et al 1994;however, see Segev and Burke 1990). For example, the sum of the currents delivered by simultaneous activation of four synapses on a distal dendrite was only 50% of the linear sum of the currents delivered by each synapse (Barrett and Crill 1974b).…”

Section: Introductionmentioning

confidence: 99%

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

Cushing¹,

Bui²,

Rose³

2005

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.

“…The electrotonic characteristics of Renshaw cells and Ia inhibitory interneurons have not previously been described. In contrast, the electrotonic properties of motoneurons, either in terms of electrotonic length, charge transfer, and/or attenuation of voltage signals have been assessed in various contexts (Bras et al 1987;Burke et al 1994;Clements and Redman 1989;Edwards and Mulloney 1984;Fleshman et al 1988;Korogod et al 2000;Nitzan et al 1990;Segev et al 1990;Svirskis et al 2001;Thurbon et al 1998;Ulrich et al 1994). However, descriptions of input resistances, current attenuations, and voltage attenuations for all parts of the dendritic tree for spinal motoneurons are incomplete [see, however, the work of Edwards and Mulloney (1984) on median gastric neurons of the stomatogastric ganglion of the spiny lobster, Bras et al (1987) and Nitzan et al (1990) for brainstem motoneurons in the cat and guinea pig, and Korogod et al (2000) for current transfer for a single cat gastrocnemius motoneuron].…”

Section: Introductionmentioning

confidence: 99%

Comparison of the Morphological and Electrotonic Properties of Renshaw Cells, Ia Inhibitory Interneurons, and Motoneurons in the Cat

Bui

Cushing

Dewey

et al. 2003

. The morphological and electrotonic properties of 4 motoneurons, 8 Ia inhibitory interneurons, and 4 Renshaw cells were compared. The morphological analysis, based on 3-D reconstructions of the cells, revealed that dendrites of motoneurons are longer and more extensively branched. Renshaw cells have dendrites that are shorter and simpler in structure. Dendrites of Ia inhibitory interneurons could be as long as those of motoneurons but the branching structure resembled that of Renshaw cells. Compartmental models were used to determine the electrotonic properties of the paths from each dendritic terminal to the soma. The attenuations of steady-state voltage changes in motoneurons were 3 and 7 times larger than in Ia inhibitory interneurons and Renshaw cells, respectively. The same relative order was observed for current attenuation and electrotonic length. The dendritic input resistances in Renshaw cells were 2 and 4 times larger than in Ia inhibitory interneurons and motoneurons, respectively. The difference in these electrotonic properties increased during higher synaptic activity as modeled by a decrease of R m . The peak amplitudes of voltage transients at sites of brief, synaptic-like changes in conductance were highly dependent on cell class and were largest in Renshaw cells and smallest in motoneurons. In combination with class-specific differences in the attenuation of transient voltage signals, this led to large differences in the peak amplitudes of somatic voltage transients. Differences in the rise times and half-widths of the voltage transients were observed as well. Thus, based on passive properties, each cell class has a unique set of input/output properties.