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Roles for multifunctional and specialized spinal interneurons during motor pattern generation in tadpoles, zebrafish larvae, and turtles.

Berkowitz A, Roberts A, Soffe SR - Front Behav Neurosci (2010)

Bottom Line: These specialized neurons can contribute by changing the way central pattern generator (CPG) activity is initiated and by altering CPG composition and operation.The combined use of multifunctional and specialized neurons is now established as a principle of organization across a range of vertebrates.Future research may reveal common patterns of multifunctionality and specialization among interneurons controlling diverse movements and whether similar mechanisms exist in higher-order brain circuits that select among a wider array of complex movements.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Oklahoma Norman, OK, USA.

ABSTRACT
The hindbrain and spinal cord can produce multiple forms of locomotion, escape, and withdrawal behaviors and (in limbed vertebrates) site-specific scratching. Until recently, the prevailing view was that the same classes of central nervous system neurons generate multiple kinds of movements, either through reconfiguration of a single, shared network or through an increase in the number of neurons recruited within each class. The mechanisms involved in selecting and generating different motor patterns have recently been explored in detail in some non-mammalian, vertebrate model systems. Work on the hatchling Xenopus tadpole, the larval zebrafish, and the adult turtle has now revealed that distinct kinds of motor patterns are actually selected and generated by combinations of multifunctional and specialized spinal interneurons. Multifunctional interneurons may form a core, multipurpose circuit that generates elements of coordinated motor output utilized in multiple behaviors, such as left-right alternation. But, in addition, specialized spinal interneurons including separate glutamatergic and glycinergic classes are selectively activated during specific patterns: escape-withdrawal, swimming and struggling in tadpoles and zebrafish, and limb withdrawal and scratching in turtles. These specialized neurons can contribute by changing the way central pattern generator (CPG) activity is initiated and by altering CPG composition and operation. The combined use of multifunctional and specialized neurons is now established as a principle of organization across a range of vertebrates. Future research may reveal common patterns of multifunctionality and specialization among interneurons controlling diverse movements and whether similar mechanisms exist in higher-order brain circuits that select among a wider array of complex movements.

No MeSH data available.


Related in: MedlinePlus

Example of a flexion reflex-selective interneuron during turtle fictive motor patterns. Activity of the interneuron (Int) during (A) a tap to the foot that evokes withdrawal (lower record expands the early part of the response shown above), (B) an electrical stimulus to the foot skin, (C) pocket scratching, and (D) forward swimming. Note that the cell is active at the start of scratch stimulation, but not during the scratch motor pattern; it is rhythmically hyperpolarized during both scratching and swimming. (E) Phase-averaged membrane potential of this neuron during scratching and swimming. HF, hip flexor; Stim., stimulus; KE, knee extensor; HE, hip extensor. Modified from Berkowitz (2007), with permission of the Society for Neuroscience.
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Figure 10: Example of a flexion reflex-selective interneuron during turtle fictive motor patterns. Activity of the interneuron (Int) during (A) a tap to the foot that evokes withdrawal (lower record expands the early part of the response shown above), (B) an electrical stimulus to the foot skin, (C) pocket scratching, and (D) forward swimming. Note that the cell is active at the start of scratch stimulation, but not during the scratch motor pattern; it is rhythmically hyperpolarized during both scratching and swimming. (E) Phase-averaged membrane potential of this neuron during scratching and swimming. HF, hip flexor; Stim., stimulus; KE, knee extensor; HE, hip extensor. Modified from Berkowitz (2007), with permission of the Society for Neuroscience.

Mentions: Another group, flexion reflex-selective neurons (Figure 10), are excited strongly and at short-latency during foot skin stimulation that evokes limb withdrawal (Figures 10A,B), but are not activated during scratching (Figure 10C) or forward swimming (Figure 10D) (Berkowitz, 2007). In most cases tested, these flexion reflex-selective neurons receive hyperpolarizing inhibition during both scratching and swimming. This hyperpolarization can be maximal during the hip flexor phase of scratching and swimming (Figure 10E), even though these neurons are strongly activated during the hip flexor burst of limb withdrawal. Flexion reflex-selective neurons have so far been found only within the dorsal horn, in contrast to multifunctional interneurons activated during scratching and swimming, which are most often found in the intermediate zone and ventral horn.


Roles for multifunctional and specialized spinal interneurons during motor pattern generation in tadpoles, zebrafish larvae, and turtles.

Berkowitz A, Roberts A, Soffe SR - Front Behav Neurosci (2010)

Example of a flexion reflex-selective interneuron during turtle fictive motor patterns. Activity of the interneuron (Int) during (A) a tap to the foot that evokes withdrawal (lower record expands the early part of the response shown above), (B) an electrical stimulus to the foot skin, (C) pocket scratching, and (D) forward swimming. Note that the cell is active at the start of scratch stimulation, but not during the scratch motor pattern; it is rhythmically hyperpolarized during both scratching and swimming. (E) Phase-averaged membrane potential of this neuron during scratching and swimming. HF, hip flexor; Stim., stimulus; KE, knee extensor; HE, hip extensor. Modified from Berkowitz (2007), with permission of the Society for Neuroscience.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2903196&req=5

Figure 10: Example of a flexion reflex-selective interneuron during turtle fictive motor patterns. Activity of the interneuron (Int) during (A) a tap to the foot that evokes withdrawal (lower record expands the early part of the response shown above), (B) an electrical stimulus to the foot skin, (C) pocket scratching, and (D) forward swimming. Note that the cell is active at the start of scratch stimulation, but not during the scratch motor pattern; it is rhythmically hyperpolarized during both scratching and swimming. (E) Phase-averaged membrane potential of this neuron during scratching and swimming. HF, hip flexor; Stim., stimulus; KE, knee extensor; HE, hip extensor. Modified from Berkowitz (2007), with permission of the Society for Neuroscience.
Mentions: Another group, flexion reflex-selective neurons (Figure 10), are excited strongly and at short-latency during foot skin stimulation that evokes limb withdrawal (Figures 10A,B), but are not activated during scratching (Figure 10C) or forward swimming (Figure 10D) (Berkowitz, 2007). In most cases tested, these flexion reflex-selective neurons receive hyperpolarizing inhibition during both scratching and swimming. This hyperpolarization can be maximal during the hip flexor phase of scratching and swimming (Figure 10E), even though these neurons are strongly activated during the hip flexor burst of limb withdrawal. Flexion reflex-selective neurons have so far been found only within the dorsal horn, in contrast to multifunctional interneurons activated during scratching and swimming, which are most often found in the intermediate zone and ventral horn.

Bottom Line: These specialized neurons can contribute by changing the way central pattern generator (CPG) activity is initiated and by altering CPG composition and operation.The combined use of multifunctional and specialized neurons is now established as a principle of organization across a range of vertebrates.Future research may reveal common patterns of multifunctionality and specialization among interneurons controlling diverse movements and whether similar mechanisms exist in higher-order brain circuits that select among a wider array of complex movements.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Oklahoma Norman, OK, USA.

ABSTRACT
The hindbrain and spinal cord can produce multiple forms of locomotion, escape, and withdrawal behaviors and (in limbed vertebrates) site-specific scratching. Until recently, the prevailing view was that the same classes of central nervous system neurons generate multiple kinds of movements, either through reconfiguration of a single, shared network or through an increase in the number of neurons recruited within each class. The mechanisms involved in selecting and generating different motor patterns have recently been explored in detail in some non-mammalian, vertebrate model systems. Work on the hatchling Xenopus tadpole, the larval zebrafish, and the adult turtle has now revealed that distinct kinds of motor patterns are actually selected and generated by combinations of multifunctional and specialized spinal interneurons. Multifunctional interneurons may form a core, multipurpose circuit that generates elements of coordinated motor output utilized in multiple behaviors, such as left-right alternation. But, in addition, specialized spinal interneurons including separate glutamatergic and glycinergic classes are selectively activated during specific patterns: escape-withdrawal, swimming and struggling in tadpoles and zebrafish, and limb withdrawal and scratching in turtles. These specialized neurons can contribute by changing the way central pattern generator (CPG) activity is initiated and by altering CPG composition and operation. The combined use of multifunctional and specialized neurons is now established as a principle of organization across a range of vertebrates. Future research may reveal common patterns of multifunctionality and specialization among interneurons controlling diverse movements and whether similar mechanisms exist in higher-order brain circuits that select among a wider array of complex movements.

No MeSH data available.


Related in: MedlinePlus