Organization of higher-order brain areas that initiate locomotor activity in larval lamprey

Paggett, Kristina C.; Jackson, Adam W.; McClellan, Andrew D.

doi:10.1016/j.neuroscience.2004.01.032

Cited by 25 publications

(55 citation statements)

References 29 publications

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“…The ejections were made by applying positive pressure pulses (10 -200 ms) through glass micropipettes using a Picospritzer (General Valve Corporation). As previously described by us and others (Paggett et al, 2004;Viana Di Prisco et al, 2005), care was taken to produce much localized actions of drugs. The drugs were ejected close to the tissue and the ejected solution was colored with Fast Green as a visual indicator for monitoring the extent of the diffusion.…”

Section: Methodsmentioning

confidence: 99%

The Contribution of Synaptic Inputs to Sustained Depolarizations in Reticulospinal Neurons

2009

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Sensory stimulation elicits sustained depolarizations in lamprey reticulospinal (RS) cells for which intrinsic properties were shown to play a crucial role. The depolarizations last up to minutes, and we tested whether the intrinsic properties required the cooperation of synaptic inputs to maintain RS cells depolarized for such long periods of time. Ascending spinal inputs to RS cells were reversibly blocked by applying xylocaine over the rostral spinal cord segments. The duration of the sustained depolarizations was markedly reduced. The membrane potential oscillations in tune with locomotor activity that were present under control condition were also abolished. The contribution of excitatory glutamatergic inputs was then assessed by applying CNQX and AP-5 over one of two simultaneously recorded homologous RS cells on each side of the brainstem. The level of sensory-evoked depolarization decreased significantly in the cell exposed to the antagonists compared with the other RS cell monitored as a control. In contrast, local application of glycine only produced a transient membrane potential hyperpolarization with a marked reduction in the amplitude of membrane potential oscillations. Locally applied strychnine did not change the duration of the sustained depolarizations, suggesting that mechanisms other than glycinergic inhibition are involved in ending the sustained depolarizations in RS cells. It is concluded that excitatory glutamatergic inputs, including ascending spinal feedback, cooperate with intrinsic properties of RS cells to maintain the cells depolarized for prolonged periods, sustaining long bouts of escape swimming.

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Section: Methodsmentioning

confidence: 99%

The Contribution of Synaptic Inputs to Sustained Depolarizations in Reticulospinal Neurons

2009

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“…In larval lamprey, reticulospinal (RS) neurons are both sufficient and necessary for initiation of locomotion (Paggett et al, 2004;Jackson et al, 2007). After a rostral spinal cord transection, axotomized RS neurons regenerate their axons for progressively greater distances caudal to the lesion with increasing recovery times (Davis and McClellan, 1994a,b), and there is a gradual recovery of locomotor function (Davis et al, 1993;McClellan, 1994) (for review, see McClellan, 1998).…”

Section: Introductionmentioning

confidence: 99%

Spinal Cord Injury Induces Changes in Electrophysiological Properties and Ion Channel Expression of Reticulospinal Neurons in Larval Lamprey

McClellan¹,

Kovalenko²,

Benes³

et al. 2008

J. Neurosci.

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In larval lamprey, hemitransections were performed on the right side of the rostral spinal cord to axotomize ipsilateral reticulospinal (RS) neurons. First, at short recovery times (2-3 weeks), uninjured RS neurons contralateral to hemitransections fired a smooth train of action potentials in response to sustained depolarization, whereas axotomized neurons fired a single short burst or short repetitive bursts. For uninjured RS neurons, the afterpotentials of action potentials had three components: fast afterhyperpolarization (fAHP), afterdepolarizing potential (ADP), and slow AHP (sAHP) that was attributable to calcium influx via high-voltage-activated (HVA) (N-and P/Q-type) calcium channels and calcium-activated potassium channels (SKKCa). For axotomized RS neurons, the fAHP was significantly larger than for uninjured neurons, and the ADP and sAHP were absent or significantly reduced. Second, at relatively long recovery times (12-16 weeks), axotomized RS neurons displayed firing patterns and afterpotentials that were similar to those of uninjured neurons. Third, mRNA levels of lamprey HVA calcium and SKKCa channels in axotomized RS neurons were significantly reduced at short recovery times and restored at long recovery times. Fourth, blocking calcium channels in uninjured RS neurons resulted in altered firing patterns that resembled those produced by axotomy. We demonstrated previously that lamprey RS neurons in culture extend neurites, and calcium influx results in inhibition of neurite outgrowth or retraction. Together, these results suggest that the downregulation of Ca 2ϩ channels in axotomized RS neurons, and the associated reduction in calcium influx, maintain intracellular calcium levels in a range that is permissive for axonal regeneration.

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“…With increasing recovery times, progressively greater numbers of axotomized descending brain neurons, of which *80% are RS neurons, extend their axons across the lesion site and for progressively greater distances below the lesion (Davis and McClellan, 1994a,b). Unidentified RS neurons, which are thought to initiate locomotor behavior (Shaw et al, 2001;Paggett et al, 2004), regenerate their axons (Zhang and McClellan, 1999), and regeneration of these injured descending axons, rather than the addition of new brain-spinal cord projections, is the main mechanism for recovery of function (Zhang et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Glutamate regulates neurite outgrowth of cultured descending brain neurons from larval lamprey

Ryan

Shotts

Hong

et al. 2007

Developmental Neurobiology

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In larval lamprey, descending brain neurons, which regenerate their axons following spinal cord injury, were isolated and examined in cell culture to identify some of the factors that regulate neurite outgrowth. Focal application of 5 mM or 25 mM L-glutamate to single growth cones inhibited outgrowth of the treated neurite, but other neurites from the same neuron were not inhibited, an effect that has not been well studied for neurons in other systems. Glutamate-induced inhibition of neurite outgrowth was abolished by 10 mM kynurenic acid. Application of high potassium media to growth cones inhibited neurite outgrowth, an effect that was blocked by 2 mM cobalt or 100 microM cadmium, suggesting that calcium influx via voltage-gated channels contributes to glutamate-induced regulation of neurite outgrowth. Application of glutamate to growth cones in the presence of 2 microM omega-conotoxin MVIIC (CTX) still inhibited neurite outgrowth, while CTX blocked high potassium-induced inhibition of neurite outgrowth. Thus, CTX blocked virtually all of the calcium influx resulting from depolarization. To our knowledge, this is the first direct demonstration that calcium influx via ligand-gated ion channels can contribute to regulation of neurite outgrowth. Finally, focal application of glutamate to the cell bodies of descending brain neurons inhibited outgrowth of multiple neurites from the same neuron, and this is the first demonstration that multiple neurites can be regulated in this fashion. Signaling mechanisms involving intracellular calcium, similar to those shown here, may be important for regulating axonal regeneration following spinal cord injury in the lamprey.

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Organization of higher-order brain areas that initiate locomotor activity in larval lamprey

Cited by 25 publications

References 29 publications

The Contribution of Synaptic Inputs to Sustained Depolarizations in Reticulospinal Neurons

The Contribution of Synaptic Inputs to Sustained Depolarizations in Reticulospinal Neurons

Spinal Cord Injury Induces Changes in Electrophysiological Properties and Ion Channel Expression of Reticulospinal Neurons in Larval Lamprey

Glutamate regulates neurite outgrowth of cultured descending brain neurons from larval lamprey

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