The control of motoneurone activity: getting all of the players on the same stage

Studies of motor control, particularly at the level of the spinal cord, have placed a high premium on the exact pathways used by segmental and descending signals en route to motoneurones. The perceived importance of the role of these pathways has inspired numerous studies that have firmly embedded the term ‘identified interneuron’ into the lexicon of spinal neuroscience (Jankowska, 2001). While not disputing the need for a precise description of the circuits linking spinal neurons, to attain a truly comprehensive understanding of the control of motor activity by these circuits requires an equally precise description of the type of sensory information that is transmitted by these circuits and the transformation of this information by the intrinsic properties of spinal neurons, especially motoneurones. Thus, the control of motoneurone activity is similar to a theatrical production in which many actors and actresses, in this case representing different circuits, types of sensory information, and intrinsic properties, occupy the same stage and engage in an interactive dialogue. When viewed from the perspective of a scientist, the challenge is to get all of these players on the same experimental stage. Electrical stimulation of peripheral nerves is a time-honoured means of defining the source and type of information delivered by muscle, joint and cutaneous afferents (Matthews, 1972). When used in conjunction with electrophysiological recordings that are synchronized to the time of the stimulus delivery, electrical stimulation of peripheral nerves offers a powerful tool to discriminate the neuronal circuits responsible for the transmission of information arising from individual classes of sensory afferents. However, this technique is ill-suited to mimic the sensory information that is generated by natural movements of the limb. Under these conditions, afferents from multiple locations and modalities will be activated together and the activity in each afferent will vary depending on the position of the limb and the kinematics of the limb movement. Thus, in the context of the desired experimental play, electrical stimulation artificially limits the number of the players that represent the sum of sensory information generated by natural movements and the multiplicity of pathways engaged in the transmission of this information. In this issue of The Journal of Physiology, Hyngstrom et al. (2008) take advantage of robotic technology to get many of the key players on the same experimental stage. In this instance, a robot was used to independently rotate the ankle, knee and hip, or all three joints at the same time. These movements generate a multimodal barrage of sensory signals that arise from sensory receptors located throughout the hindlimb. A small number of investigators have previously used robots to examine the sensory responses of ascending tract neurons in the spinal cord (e.g. Bosco et al. 1996). However, Hyngstrom and colleagues have applied this technology in a way that allows us to listen to the dialogue between the many players representing sensory information, circuits, and importantly, the intrinsic properties of motoneurones. The dendrites of motoneurones possess an array of intrinsic conductances, including a set of voltage-dependent sodium and calcium channels that generate persistent inward currents (PICs, Heckman et al. 2003). PICs are readily activated or deactivated by sensory stimuli in decerebrate animals due to the actions of monoamines released by descending pathways. However, in the acute period following spinal transection, modulation of PICs by segmental circuits is greatly diminished. Thus, by comparing the current reaching the soma of ankle or knee extensor motoneurones in decerebrate and acutely spinalized animals during robotically controlled limb movements, Hyngstrom and colleagues were able to isolate the role of PICs (i.e. one of the intrinsic property players) during activation of multiple spinal circuits by physiologically relevant sensory information (represented by several players). The results of the study are described in the form of movement related receptive fields. These fields are defined by the strength of the signals received from different joints. The data suggest that PICs reduce the dimensions of movement related receptive fields. For example, in the absence of PIC modulation by descending monoaminergic systems, rotations at the hip generate large synaptic currents in ankle extensor motoneurones. These currents are greatly reduced in the presence of PIC modulation. It is perhaps ironic, given the original goal of recruiting more key players to the stage, that the interaction between these players causes some of the new members of the cast to lose their voices. This outcome may indicate that the players representing descending monoaminergic systems and PICs are the stars in this play. It is tempting to speculate that the more potent actions of intraspinal monoaminergic systems in chronic models of spinal cord injury may raise the voices of excitatory muscle afferent circuits and thereby contribute to muscle spasms (Harvey et al. 2006). However, the words for this play have yet to be written.

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