Adjustable Amplification of Synaptic Input in the Dendrites of Spinal Motoneurons In Vivo

Abstract

The impact of neuromodulators on active dendritic conductances was investigated by the use of intracellular recording techniques in spinal motoneurons in the adult cat. The well known lack of voltage control of dendritic regions during voltage clamp applied at the soma was used to estimate dendritic amplification of a steady monosynaptic input generated by muscle spindle Ia afferents. In preparations deeply anesthetized with pentobarbital, Ia current either decreased with depolarization or underwent a modest increase at membrane potentials above Ϫ40 mV. In unanesthetized decerebrate preparations (which have tonic activity in axons originating in the brainstem and releasing serotonin or norepinephrine), active dendritic currents caused strong amplification of Ia input. In the range of Ϫ50 to Ϫ40 mV, peak Ia current was over four times as large as that in the pentobarbital-anesthetized preparations. Exogenous administration of a noradrenergic agonist in addition to the tonic activity further enhanced amplification (sixfold increase). Amplification was not seen in preparations with spinal transections. Overall, the dendritic amplification with moderate or strong neuromodulatory drive was estimated to be large enough to allow the motoneurons innervating slow muscle fibers to be driven to their maximum force levels by remarkably small synaptic inputs. In these cells, the main role of synaptic input may be to control the activation of a highly excitable dendritic tree. The neuromodulatory control of synaptic amplification provides motor commands with the potential to adjust the level of amplification to suit the demands of different motor tasks. Key words: motoneuron; spinal cord; neuromodulation; electrophysiology; serotonin; norepinephrine; plateau potential; bistable; dendritic amplificationVoltage-sensitive conductances within the dendritic tree of the postsynaptic neuron play a major role in synaptic integration (Johnston et al., 1996;Yuste and Tank, 1996). Many types of voltage-sensitive conductances are under the control of neuromodulatory inputs acting via second messenger systems. Thus, the potential exists for the neuromodulatory inputs to control synaptic integration by altering the activation of voltage-sensitive currents in the dendrites of neurons.The spinal motoneuron is subject to potent neuromodulatory control by axons that originate in the brainstem and release either serotonin (5-HT) or norepinephrine (NE) (Hounsgaard et al., 1988;Takahashi and Berger, 1990;Wang and Dun, 1990;White et al., 1991;Binder et al., 1996). In the presence of these neuromodulators, motoneurons exhibit a persistent inward current (Hounsgaard and Kiehn, 1989;Svirskis and Hounsgaard, 1998;Lee and Heckman, 1999a). The composition of this current may vary in different types of motoneurons (Hounsgaard and Kiehn, 1989;Hsiao and Chandler, 1995;Zhang et al., 1995;Lee and Heckman, 1998b). In spinal motoneurons in the adult cat, the total persistent inward current (I PIC ) is exceedingly large Heckman, 1998a, 1999a). Activation of I...

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“…Serotonergic (5-HT) neurons of the raphe nucleus and noradrenergic (NE) neurons from the locus coeruleus may contribute much of this basal excitatory input. 19,20 5-HT and NE act on spinal motor neurons yielding plateau potentials, which may amplify excitatory inputs including reflex inputs. [21][22][23] Plateau potentials originate on dendrites and amplify excitatory inputs up to six-fold, thus leading to sustained firing with minimal excitatory input.…”

Prediction of upper limb muscle activity from motor cortical discharge during reaching

“…To the extent that these inputs were independent of, or significantly nonlinear functions of cortical activity, their effects on muscle activation would be difficult to predict. Furthermore, plateau potentials mediated by persistent inward calcium channels may actually contribute significantly more net current than the synaptic inputs that trigger them (Lee and Heckman 2000). It has been suggested that they may function as a powerful nonlinear amplifier of synaptic input.…”

Synaptic Release of Serotonin Induced by Stimulation of the Raphe Nucleus Promotes Plateau Potentials in Spinal Motoneurons of the Adult Turtle

“…Many studies suggest that plateau potentials are recruited under physiological conditions (Eken and Kiehn, 1989;Kiehn and Eken, 1997;Gorassini et al, 1999;Alaburda and Hounsgaard, 2003;Perrier and Tresch, 2005). They may contribute to behaviors by amplifying synaptic inputs to motoneurons (Conway et al, 1988;Hultborn, 1999;Lee and Heckman, 2000) or by specifying the temporal details of motor output (Perrier and Tresch, 2005).…”