Trends in Neurosciences
ReviewGap junctions and motor behavior
Section snippets
Electrical coupling between developing spinal motor neurons can coordinate a motor output in the absence of fast chemical synaptic transmission
It has long been known that motor neurons in the developing spinal cord are electrically coupled. This has been demonstrated in both non-limbed vertebrates 3, 6, 7 and mammals 8, 9, 10 (Box 1). Electrical coupling is likely to synchronize the activity of motor neurons, a role similar to that proposed for electrical GJC between neighboring cells in other areas of the CNS [11]. In a recent study, this hypothesis was tested directly by examining the motor pattern generating capability of the
Electrical coupling among motor neurons is restricted to functional groups
Several lines of evidence suggest that the electrical coupling among spinal motor neurons is relatively restricted: there is no coupling between flexor and extensor motor neurons and small or no coupling potentials between motor neurons innervating synergistic muscles 9, 23. In contrast, large electrical coupling potentials are consistently found between motor neurons innervating homonymous muscles. The gap junction and NMDA mediated oscillations described above were similarly anatomically
Synchrony
An obvious consequence of electrical coupling among motor neurons is that it will tend to synchronize their firing. Synchronized firing is a widespread phenomenon in the mammalian brain 25, 26, including the motor cortex [27], respiratory motor neurons 28, 29, 30 and limb motor neurons 31, 32. Several recent studies have addressed the role of GJC in synchronous motor neuron firing directly and reached conflicting results regarding the role of GJC for motor neuron synchronization. One study was
Electrical coupling between pre-motor interneurons
Gap junctions among interneurons play an important role for the function of neural networks generating rhythmic motor outputs in invertebrates 42, 43. Few studies have addressed this issue in vertebrate motor systems. Perhaps one reason for this is that it is technically more difficult to demonstrate electrical coupling between interneurons because it most often requires paired recordings.
Using paired recordings, Rekling et al. [24] demonstrated bi-directional electrical coupling between
Electrical coupling in adult mammalian motor systems
In the above description we have concentrated on data from pre- and early postnatal animals. Several studies have indicated that electrical GJC, although present in spinal cords from adult aquatic vertebrates (frog [51], lamprey [48] and goldfish [49]), are transient in nature in the mammalian spinal cord 3, 4, 5. This has led to the notion that electrical gap junctions might not play any role in coordinating motor acts in adult mammals. Below we will review evidence which suggests that this
Conclusions
As detailed in this review, there have been several recent studies examining the role of gap junctions in motor systems. These studies have demonstrated the presence of gap junctions between neurons at many levels of the motor system, in both motor neurons and in premotor pattern generating circuits. Although gap junctions are clearly prevalent in early development, there is also considerable evidence that, at least anatomically, the substrates for gap junctions are present in adults as well.
Acknowledgements
We would like to acknowledge Henning Schmalbruch for posing the idea about GJC and fasciculations. O.K. is supported by NINDS and Karolinska Institutet.
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2016, Current Opinion in NeurobiologyCitation Excerpt :A similar picture was confirmed in the vertebrates [62]. Electrical coupling among MNs that innervate synergistic muscles [1] can be simply interpreted: synchronic activation of MNs can grant a more precise coactivation of muscles. However, electrical synapses could be expressed among MNs that do not (always) fire in synchrony [36,37].
Motor neuron cell bodies are actively positioned by Slit/Robo repulsion and Netrin/DCC attraction
2015, Developmental BiologyCitation Excerpt :Because of their position near the floor plate, neural progenitors in a narrow column are exposed to a specific concentration of Sonic hedgehog morphogen and respond by expressing a cascade of transcriptional regulators that specifies their differentiation as motor neurons and clustering into motor nuclei (Briscoe and Ericson, 2001; Briscoe et al., 1999; Osterfield et al., 2003). The position of motor neuron clusters is important for the function of motor circuits, because motor neuron position influences where their axons exit the CNS toward their peripheral muscle targets (Bravo-Ambrosio and Kaprielian, 2011), which synaptic inputs they receive from sensory and other neurons (Chang and Balice-Gordon, 2000; Fritzsch et al., 1993; Song and Pfaff, 2005), and whether neighboring neurons become electrically coupled within motor pools (Brenowitz et al., 1983; Kiehn and Tresch, 2002). Motor neuron cell bodies can shift locally within their nucleus to settle into topographic order (Leber and Sanes, 1995), with these shifts regulated by Reelin and cadherin signaling (Demireva et al., 2011; Palmesino et al., 2010; Price et al., 2002; Yip et al., 2000).