Spinobulbar Neurons in Lamprey: Cellular Properties and Synaptic Interactions

Einum, James F.; Buchanan, James T.

doi:10.1152/jn.01331.2005

Cited by 14 publications

(17 citation statements)

References 43 publications

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“…Squares and circles represent commissural excitatory interneurons and commissural caudally projecting interneurons, respectively. Buchanan 2006;Vinay et al 1998), but as much as 86% of the axons displayed significant locomotor-related activity. Consequently, one should anticipate that the phasic activity pattern should be distributed in all parts of the cycle, when considering the results with the inhibitory and excitatory INs.…”

Section: Activity In Unidentified Commissural Axonsmentioning

confidence: 99%

The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey

Biró

Hill²,

Grillner³

2008

Journal of Neurophysiology

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Biró Z, Hill RH, Grillner S. The activity of spinal commissural interneurons during fictive locomotion in the lamprey. J Neurophysiol 100: 716 -722, 2008. First published May 28, 2008 doi:10.1152/jn.90206.2008. Commissural interneurons in the lamprey coordinate activity of the hemisegmental oscillators to ensure proper left-right alternation during swimming. The activity of interneuronal axons at the ventral commissure was studied together with potential target motoneurons during fictive locomotion in the isolated lamprey spinal cord. To estimate the unperturbed activity of the interneurons, axonal recordings were chosen because soma recordings inevitably will affect the level of membrane depolarization and thereby spike initiation. Of 227 commissural axons recorded during locomotor activity, 14 produced inhibitory and 3 produced excitatory postsynaptic potentials (PSPs) in target motoneurons. The axons typically fired multiple spikes per locomotor cycle, with ϳ10 Hz sustained frequency. The average shortest spike interval in a burst corresponded to an instantaneous frequency of ϳ50 Hz for both the excitatory and inhibitory axons. The maximum number of spikes per locomotor cycle was inversely related to the locomotor frequency, in accordance with previous observations in the spinal hemicord preparation. In axons that fired multiple spikes per cycle, the mean interspike intervals were in the range in which the amplitude of the slow afterhyperpolarization (sAHP) is large, providing further support for the role of the sAHP in spike timing. One hundred ninety-five axons (86%) fired rhythmically during fictive locomotion, with preferred phase of firing distributed over either the segmental locomotor burst phase (40% of axons) or the transitional phase (between bursts; 60%). Thus in lamprey commissural interneurons, we found a broad distribution of firing rates and phases during fictive locomotion.

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Section: Activity In Unidentified Commissural Axonsmentioning

confidence: 99%

The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey

Biró

Hill²,

Grillner³

2008

Journal of Neurophysiology

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“…This feedback is conveyed to reticulospinal neurons via ascending spinobulbar neurons (15)(16)(17)(18)(19)(20) that provide an "efference copy" regarding the cycle-to-cycle activity in the locomotor network. Spinobulbar neurons (21) provide the excitatory and inhibitory drive to reticulospinal neurons, resulting in modulation of their activity in phase with the ipsilateral rostral parts of the spinal cord (21,22) and this forms a closed spinoreticulo-spinal loop (17).…”

mentioning

confidence: 99%

Gating of steering signals through phasic modulation of reticulospinal neurons during locomotion

Kozlov

Kardamakis

Kotaleski

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The neural control of movements in vertebrates is based on a set of modules, like the central pattern generator networks (CPGs) in the spinal cord coordinating locomotion. Sensory feedback is not required for the CPGs to generate the appropriate motor pattern and neither a detailed control from higher brain centers. Reticulospinal neurons in the brainstem activate the locomotor network, and the same neurons also convey signals from higher brain regions, such as turning/steering commands from the optic tectum (superior colliculus). A tonic increase in the background excitatory drive of the reticulospinal neurons would be sufficient to produce coordinated locomotor activity. However, in both vertebrates and invertebrates, descending systems are in addition phasically modulated because of feedback from the ongoing CPG activity. We use the lamprey as a model for investigating the role of this phasic modulation of the reticulospinal activity, because the brainstem-spinal cord networks are known down to the cellular level in this phylogenetically oldest extant vertebrate. We describe how the phasic modulation of reticulospinal activity from the spinal CPG ensures reliable steering/turning commands without the need for a very precise timing of on-or offset, by using a biophysically detailed large-scale (19,600 model neurons and 646,800 synapses) computational model of the lamprey brainstem-spinal cord network. To verify that the simulated neural network can control body movements, including turning, the spinal activity is fed to a mechanical model of lamprey swimming. The simulations also predict that, in contrast to reticulospinal neurons, tectal steering/ turning command neurons should have minimal frequency adaptive properties, which has been confirmed experimentally.large-scale modeling | compartmental modelling | full-scale model | MLR

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“…Mutual excitatory coupling among reticulospinal neurons has been shown in Xenopus tadpoles (Li et al 2006) and, if present in lamprey, would enhance brain stem-induced activity. Mutual excitation between reticulospinal neurons and some excitatory spinobulbar neurons has been shown in lamprey (Einum and Buchanan 2006). Second, the density of spinobulbar neurons is highest in the most rostral spinal segments and falls sharply with distance from the brain stem (Vinay et al 1998b).…”

Section: Discussionmentioning

confidence: 97%

“…Paired intracellular recordings have further shown that monosynaptic interactions from spinobulbar neurons to reticulospinal neurons exist and that these interactions can be either excitatory or inhibitory. Both the excitatory and the inhibitory spinobulbar neurons can project either ipsilaterally or contralaterally to the brain stem (Einum and Buchanan 2006). Although direct inputs clearly exist, indirect inputs to reticulospinal neurons cannot be completely ruled out, even in the presence of high-divalent cation solution.…”

Section: Discussionmentioning

confidence: 99%

“…The likeliest explanation is that all of the oscillations originate mainly from the most rostral spinal segments, where there is the highest density of spinobulbar neurons, and the out-of-phase peaks represent input from the locomotor networks on the opposite side of the spinal cord. Since in the rostral spinal cord both ipsilateral and contralateral ascending spinobulbar neurons exist (Einum and Buchanan 2006;Vinay et al 1998b), can be either excitatory or inhibitory, and are rhythmically active during locomotion (Einum and Buchanan 2006), the anatomical substrate exists for input to reticulospinal neurons from the contralateral locomotor networks. The amplitude of the out-of-phase peak could be quite variable in the same identified neuron from preparation to preparation.…”

Section: Discussionmentioning

confidence: 99%

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Spinal locomotor inputs to individually identified reticulospinal neurons in the lamprey

Buchanan

2011

Journal of Neurophysiology

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Locomotor feedback signals from the spinal cord to descending brain stem neurons were examined in the lamprey using the uniquely identifiable reticulospinal neurons, the Müller and Mauthner cells. The same identified reticulospinal neurons were recorded in several preparations, under reduced conditions, to address whether an identified reticulospinal neuron shows similar locomotor-related oscillation timing from animal to animal and whether these timing signals can differ significantly from other identified reticulospinal neurons. Intracellular recordings of membrane potential in identified neurons were made in an isolated brain stem-spinal cord preparation with a high-divalent cation solution on the brain stem to suppress indirect neural pathways and with D-glutamate perfusion to the spinal cord to induce fictive swimming. Under these conditions, the identified reticulospinal neurons show significant clustering of the timings of the peaks and troughs of their locomotor-related oscillations. Whereas most identified neurons oscillated in phase with locomotor bursting in ipsilateral ventral roots of the rostral spinal cord, the B1 Müller cell, which has an ipsilateral descending axon, and the Mauthner cell, which has a contralateral descending axon, both had oscillation peaks that were out of phase with the ipsilateral ventral roots. The differences in oscillation timing appear to be due to differences in synaptic input sources as shown by cross-correlations of fast synaptic activity in pairs of Müller cells. Since the main source of the locomotor input under these experimental conditions is ascending neurons in the spinal cord, these experiments suggest that individual reticulospinal neurons can receive locomotor signals from different subsets of these ascending neurons. This result may indicate that the locomotor feedback signals from the spinal locomotor networks are matched in some way to the motor output functions of the individual reticulospinal neurons, which include command signals for turning and for compensatory movements.

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Spinobulbar Neurons in Lamprey: Cellular Properties and Synaptic Interactions

Cited by 14 publications

References 43 publications

The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey

The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey

Gating of steering signals through phasic modulation of reticulospinal neurons during locomotion

Spinal locomotor inputs to individually identified reticulospinal neurons in the lamprey

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