Descending brain neurons in larval lamprey: Spinal projection patterns and initiation of locomotion

Shaw, Albert C.; Jackson, Adam W.; Holmes, Tamra; Thurman, Suzie; Davis, Gwendolyn; McClellan, Andrew D.

doi:10.1016/j.expneurol.2010.05.016

Cited by 22 publications

(25 citation statements)

References 82 publications

(167 reference statements)

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“…The number of processes in the dorsomedial region is recovered at 2 wpl both rostral and caudal to the site of injury. Most of the processes of the lateral region correspond to small RS glutamatergic neurons of several rhombencephalic nuclei (anterior, middle and posterior rhombencephalic reticular nuclei41 and the postero-lateral vagal group42) and to processes of the cells of the lateral population of the spinal cord. Based on the know timing of regeneration of descending neurons (see above), the recovery of the number of processes at 2 wpl in the caudal stump has to be attributed to the intrinsic lateral spinal neurons.…”

Section: Discussionmentioning

confidence: 99%

“…Processes of the dorsomedial region comprise the dorsal column (DC) (constituted by axons of the primary sensory dorsal cells and dorsal root ganglion cells4344) as well as the descending trigeminal tract, which is located next to the DC45, and processes of the cells of the dorsal population. In addition, some descending axons from the mesencephalic reticular nucleus (MRN) and the antero-lateral vagal group (ALV), which project to the medial (dorsal and/or ventral) spinal region42, may also descend in this region. Axons of the dorsal cells have been shown to have bad regenerative capacity14 and previous studies have shown that the projections from the ALV do not recover to normal levels even at 32 wpl, whereas axons of the MRN show good recovery at 32 wpl16.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Fernández-López

Barreiro‐Iglesias

Rodicio

2016

Sci Rep

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Lampreys recover locomotion following a spinal cord injury (SCI). Glutamate is necessary to initiate and control locomotion and recent data suggest a crucial role for intraspinal neurons in functional recovery following SCI. We aimed to determine whether, in lampreys, axotomized spinal glutamatergic neurons, which lose glutamate immunoreactivity immediately after SCI, recover it later on and to study the long-term evolution and anatomical recovery of the spinal glutamatergic system after SCI. We used glutamate immunoreactivity to study changes in the glutamatergic system, tract-tracing to label axotomized neurons and TUNEL labelling to study cell death. Transections of the cord were made at the level of the fifth gill. TUNEL experiments indicated that cell death is a minor contributor to the initial loss of glutamate immunoreactivity. At least some of the axotomized neurons lose glutamate immunoreactivity, survive and recover glutamate immunoreactivity 1 week post-lesion (wpl). We observed a progressive increase in the number of glutamatergic neurons/processes until an almost complete anatomical recovery at 10 wpl. Among all the glutamatergic populations, the population of cerebrospinal fluid-contacting cells is the only one that never recovers. Our results indicate that full recovery of the glutamatergic system is not necessary for the restoration of function in lampreys.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Fernández-López

Barreiro‐Iglesias

Rodicio

2016

Sci Rep

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“…Inputs from these regions converge on reticulospinal neurons, which in turn activate spinal networks (El Manira et al, 1997;Dubuc et al, 2008;Shaw et al, 2010). However, in all these cases, the expression of locomotor activity required that these centers are stimulated continuously and the activity declined rapidly upon termination of the stimulation.…”

Section: Discussionmentioning

confidence: 99%

Initiation of Locomotion in Adult Zebrafish

Kyriakatos

Mahmood²,

Ausborn³

et al. 2011

Journal of Neuroscience

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Motor behavior is generated by specific neural circuits. Those producing locomotion are located in the spinal cord, and their activation depends on descending inputs from the brain or on sensory inputs. In this study, we have used an in vitro brainstem-spinal cord preparation from adult zebrafish to localize a region where stimulation of descending inputs can induce sustained locomotor activity. We show that a brief stimulation of descending inputs at the junction between the brainstem and spinal cord induces long-lasting swimming activity. The swimming frequencies induced are remarkably similar to those observed in freely moving adult fish, arguing that the induced locomotor episode is highly physiological. The motor pattern is mediated by activation of ionotropic glutamate and glycine receptors in the spinal cord and is not the result of synaptic interactions between neurons at the site of the stimulation in the brainstem. We also compared the activity of motoneurons during locomotor activity induced by electrical stimulation of descending inputs and by exogenously applied NMDA. Prolonged NMDA application changes the shape of the synaptic drive and action potentials in motoneurons. When escape activity occurs, the swimming activity in the intact zebrafish was interrupted and some of the motoneurons involved became inhibited in vitro. Thus, the descending inputs seem to act as a switch to turn on the activity of the spinal locomotor network in the caudal spinal cord. We propose that recurrent synaptic activity within the spinal locomotor circuits can transform a brief input into a well coordinated and long-lasting swimming pattern.

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“…Many of the RS neurons that initiate locomotion project their descending axons primarily in the lateral parts of the spinal cord (McClellan, 1988; Shaw et al, 2010). In larval lamprey, DLM- or VMD-initiated locomotor activity usually is abolished or significantly attenuated when neural activity is blocked in reticular nuclei (Paggett et al, 2004), and RS neurons receive direct synaptic inputs from the VMD and DLM locomotor areas (El Manira et al, 1997; Paggett et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Localization, pharmacology, and organization of brain locomotor areas in larval lamprey

Jackson

McClellan

2011

Neuroscience

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In larval lamprey, spinal locomotor activity can be initiated by pharmacological microstimulation from the following higher order brain locomotor areas (Paggett et al., 2004; Jackson et al., 2007): rostrolateral rhombencephalon (RLR); ventromedial diencephalon (VMD); or dorsolateral mesencephalon (DLM). In the present study, pharmacological microstimulation with excitatory amino acids (EAAs) or their agonists in the brains of in vitro brain/spinal cord preparations was used to determine the sizes, pharmacology, and organization of these locomotor areas. First, the RLR, DLM and VMD locomotor areas were confined to relatively small areas of the brain, and stimulation as little as 50 μm outside these areas was ineffective or elicited tonic or uncoordinated motor activity. Second, pharmacological stimulation with NMDA, kainate, or AMPA in the VMD or DLM reliably initiated well-coordinated spinal locomotor activity. In the RLR, stimulation with all three ionotropic EAA receptor agonists could initiate spinal locomotor activity, but NMDA or AMPA was more reliable than kainate. Third, with synaptic transmission blocked only in the brain, stimulation in the RLR, VMD, or DLM no longer initiated spinal locomotor activity, suggesting that these locomotor areas do not directly activate spinal locomotor networks. Fourth, following a complete transection at the mesencephalon-rhombencephalon border, stimulation in the RLR no longer initiated spinal motor activity. Thus, the RLR locomotor area does not appear able to initiate spinal locomotor activity by neural circuits confined entirely within the rhombencephalon but requires more rostral neural centers, such as those in the VMD and DLM, as previously proposed (Paggett et al., 2004).

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Descending brain neurons in larval lamprey: Spinal projection patterns and initiation of locomotion

Cited by 22 publications

References 82 publications

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Initiation of Locomotion in Adult Zebrafish

Localization, pharmacology, and organization of brain locomotor areas in larval lamprey

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