Neuronal Population Activity in Spinal Motor Circuits: Greater Than the Sum of Its Parts

Berg, Rune W.

doi:10.3389/fncir.2017.00103

Cited by 13 publications

(12 citation statements)

References 75 publications

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“…In a recent study, Petersen and Berg ( 2016 ) demonstrated that the firing rate of populations of neurons from the turtle spinal cord is normally distributed on a log-scale (lognormal) (see also Berg, 2017 ). We examined whether the firing rate before and after the onset of movement for the extensor, intermediate, and flexor interneurons is also lognormally distributed.…”

Section: Resultsmentioning

confidence: 99%

“…The studies performed by Petersen and Berg ( 2016 ) contribute to our understanding of the spinal circuitry responsible for scratching in a new perspective. These authors demonstrated for the first time that the behavior of neural populations in the spinal cord could not be properly described by the mean and standard deviation of their firing rate (Berg, 2017 ). They found that the firing rate of spinal neurons during different forms of scratching is lognormally distributed (Petersen and Berg, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

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The Spinal Neurons Exhibit an ON-OFF and OFF-ON Firing Activity Around the Onset of Fictive Scratching Episodes in the Cat

Cuellar

Valdovinos

Huidobro

et al. 2018

Front. Cell. Neurosci.

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In a previous report, we found neurons with ON-OFF and OFF-ON firing activity in the obex reticular formation during scratching. The aim of the present study was to examine whether the spinal neurons also exhibit this type of activity in relation to the “postural stage” of fictive scratching in the cat. We found that the extensor and intermediate scratching neurons exhibit an ON-OFF firing rate; conversely, the flexor neurons show an OFF-ON activity, relative to every scratching episode. These patterns of spiking activity are similar to those found in neurons from the obex reticular formation during scratching. Our findings provide support to the following hypotheses. First, there is a possible functional link between supraspinal and spinal, ON-OFF and OFF-ON neuronal groups. Second, the fictive goal-directed motor action to maintain the fictive “postural stage” of the hindlimb during fictive scratching is associated with the neuronal tonic activity of the OFF-ON spinal neurons, whereas the ON-OFF spinal neurons are associated with an extensor tone that occurred prior the postural stage.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The Spinal Neurons Exhibit an ON-OFF and OFF-ON Firing Activity Around the Onset of Fictive Scratching Episodes in the Cat

Cuellar

Valdovinos

Huidobro

et al. 2018

Front. Cell. Neurosci.

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“…In this context, shunting ipsilateral inhibition might serve to enforce tight temporal control over spike timing via shortening membrane time constants. Alternatively or in addition, ipsilateral inhibition might function as a form of gain control to prevent saturation, analogous to somatic inhibition in hippocampus and cortex [11, 63, 64].…”

Section: Discussionmentioning

confidence: 99%

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

Callahan¹,

Roberts²,

Sengupta³

et al. 2019

Preprint

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10The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, 11 models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal 12 alternation between left and right sides or flexors and extensors. However, recent work has 13shown that inhibition also increases coincident with excitation during contraction. Here, using 14 larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-15 extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines 16 we define two stable subclasses with distinct neurotransmitter and morphological properties. 17These two V2b subclasses make direct synapses onto motor neurons with differential targeting to 18 slower and faster circuits. In vivo, optogenetic suppression of V2b activity leads to increases in 19 locomotor speed. We conclude that V2b neurons exert speed-specific influence over axial motor 20 circuits throughout the rostrocaudal axis. Together, these results indicate a new role for 21 ipsilateral inhibition in speed control. 22 46In-phase inhibition is thought to derive from two spinal interneuron classes, the V1 and V2b 47 populations. The V1 population includes Renshaw cells [15, 16], which provide recurrent 48 inhibition onto motor neurons with potentially significant shunting effects [17]. To date, most 49 analysis of drive from V2b neurons has focused on the shared contributions of V1s and V2bs to 50 reciprocal inhibition governing flexor/extensor alternation in limbed animals [18][19][20]. However, 51 this does not shed light on potential functions of ipsilateral inhibition in gain control for 52 regulation of motor neuron firing during contraction, as opposed to suppression of motor neuron 53 firing during extension. 54 55In-phase inhibition increases in amplitude for faster locomotor movements [10] suggesting a 56 potential role in speed control. Here we investigated whether V2b neurons could indeed provide 57 direct inhibition to motor neurons for speed control, taking advantage of the speed-dependent 58 organization of zebrafish motor circuits [21][22][23]. V2b neurons are good candidates for in-phase 59 gain control because they are exclusively inhibitory in mouse and zebrafish [24] with ipsilateral, 60 descending axons within the spinal cord [18, 25]. They arise from a final progenitor division that 61 produces pairs of V2a and V2b neurons [26]. Given the role of V2a neurons in triggering motor 62 output [27, 28], particularly through speed-specific circuits for titrating levels of motor excitation 63[4, 29-31], it seems plausible that their sister V2b neurons exert an opposing, inhibitory role in 64 speed control. However, the V2b class has not been well characterized at anatomical or 65 neurochemical levels outside of very early development. 66 67 5Here, we define two subclasses of V2b neurons in larval zebrafish based on differential 68 transmitter expression and anatomy, and further show that these neurons directly inhibit a...

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“…This phenomenon is widespread in the central nervous system, and there is evidence that neurons interact through phase resetting to establish a time frame for information encoding and decoding (Canavier, 2015), among other behaviors. In particular, the analysis of phase resetting is of interest in circuits known as central pattern generators (CPGs) because the elucidation of their structure and organization is a work in progress and because the cooperation between CPGs is poorly understood (Berg et al, 2007; Stuart and Hultborn, 2008; McCrea and Rybak, 2008; Harris-Warrick, 2010; Enriquez-Denton et al, 2012; Tsuruyama et al, 2013; Grillner and El Manira, 2015; Kiehn, 2016; Ramirez et al, 2016; Pujala et al, 2016; Berg, 2017; Stein, 2018; Steuer and Guertin, 2019).…”

Section: Introductionmentioning

confidence: 99%

Resetting the Respiratory Rhythm with a Spinal Central Pattern Generator

Meza

Huidobro

Moreno-Castillo

et al. 2019

eNeuro

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There is evidence that a variety of central and afferent stimuli, including swallowing, can produce phase resetting in the respiratory rhythmicity. Also, there are reports about the intrinsic linkage between locomotion and respiration. However, little is known about the interaction between the central pattern generators (CPGs) for scratching and respiration. The present study aims to examine whether the activation of scratching CPG produces phase resetting of the respiratory rhythm. We employed decerebrate cats to apply brief tactile stimuli to the pinna during the inspiratory-expiratory transition. We observed that those stimuli to the pinna not eliciting fictive scratching did not reset the respiratory rhythm. However, when the pinna stimuli elicited fictive scratching, then the respiratory rhythm exhibited a significant phase resetting. We also found interneurons in the medulla oblongata exhibiting phase resetting related to scratching-CPG episodes. This second finding suggests that this type of resetting involves brainstem components of the respiratory CPG. These results shed new light on the resetting action from a spinal CPG on the respiratory rhythm.

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Neuronal Population Activity in Spinal Motor Circuits: Greater Than the Sum of Its Parts

Cited by 13 publications

References 75 publications

The Spinal Neurons Exhibit an ON-OFF and OFF-ON Firing Activity Around the Onset of Fictive Scratching Episodes in the Cat

The Spinal Neurons Exhibit an ON-OFF and OFF-ON Firing Activity Around the Onset of Fictive Scratching Episodes in the Cat

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

Resetting the Respiratory Rhythm with a Spinal Central Pattern Generator

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