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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 turtle scratch-specialized interneuron during fictive motor patterns. Activity of the interneuron (Int) during (A) rostral scratching, (B) caudal scratching, and (C,D) forward swimming. Note that the interneuron is hyperpolarized for several seconds beyond the swim-evoking stimulus, as the motor pattern continues. KE, knee extensor; HF, hip flexor; HE, hip extensor; Stim., stimulus. Modified from Berkowitz (2008), with permission of the American Physiological Society.
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Figure 9: Example of a turtle scratch-specialized interneuron during fictive motor patterns. Activity of the interneuron (Int) during (A) rostral scratching, (B) caudal scratching, and (C,D) forward swimming. Note that the interneuron is hyperpolarized for several seconds beyond the swim-evoking stimulus, as the motor pattern continues. KE, knee extensor; HF, hip flexor; HE, hip extensor; Stim., stimulus. Modified from Berkowitz (2008), with permission of the American Physiological Society.

Mentions: When forward swimming and limb withdrawal are brought into the picture, however, the idea that a single set of multifunctional interneurons triggers all of these behaviors is not consistent with all of the data (Berkowitz, 2002, 2007, 2008). It is true that many spinal interneurons are activated during both scratching and forward swimming motor patterns (scratch/swim neurons) (Berkowitz, 2002, 2008) (Figure 7). Many are also activated during limb withdrawal (Berkowitz, 2005). In addition to these multifunctional interneurons, however, there are at least two functionally defined categories of behaviorally specialized interneurons. One group, scratch-specialized neurons (Figure 9), are activated during all forms of scratching but are not activated during forward swimming (Berkowitz, 2002, 2008). In at least some cases, scratch-specialized interneurons receive hyperpolarizing inhibition during forward swimming (Figures 9C,D) (Berkowitz, 2008). As a group, scratch-specialized neurons are less likely than scratch/swim neurons to be activated during ipsilateral or contralateral limb withdrawal (Berkowitz, 2002). Thus, to some extent, scratch/swim neurons are general “multipurpose” limb motor control neurons while scratch-specialized neurons are quite specialized.


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 turtle scratch-specialized interneuron during fictive motor patterns. Activity of the interneuron (Int) during (A) rostral scratching, (B) caudal scratching, and (C,D) forward swimming. Note that the interneuron is hyperpolarized for several seconds beyond the swim-evoking stimulus, as the motor pattern continues. KE, knee extensor; HF, hip flexor; HE, hip extensor; Stim., stimulus. Modified from Berkowitz (2008), with permission of the American Physiological Society.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 9: Example of a turtle scratch-specialized interneuron during fictive motor patterns. Activity of the interneuron (Int) during (A) rostral scratching, (B) caudal scratching, and (C,D) forward swimming. Note that the interneuron is hyperpolarized for several seconds beyond the swim-evoking stimulus, as the motor pattern continues. KE, knee extensor; HF, hip flexor; HE, hip extensor; Stim., stimulus. Modified from Berkowitz (2008), with permission of the American Physiological Society.
Mentions: When forward swimming and limb withdrawal are brought into the picture, however, the idea that a single set of multifunctional interneurons triggers all of these behaviors is not consistent with all of the data (Berkowitz, 2002, 2007, 2008). It is true that many spinal interneurons are activated during both scratching and forward swimming motor patterns (scratch/swim neurons) (Berkowitz, 2002, 2008) (Figure 7). Many are also activated during limb withdrawal (Berkowitz, 2005). In addition to these multifunctional interneurons, however, there are at least two functionally defined categories of behaviorally specialized interneurons. One group, scratch-specialized neurons (Figure 9), are activated during all forms of scratching but are not activated during forward swimming (Berkowitz, 2002, 2008). In at least some cases, scratch-specialized interneurons receive hyperpolarizing inhibition during forward swimming (Figures 9C,D) (Berkowitz, 2008). As a group, scratch-specialized neurons are less likely than scratch/swim neurons to be activated during ipsilateral or contralateral limb withdrawal (Berkowitz, 2002). Thus, to some extent, scratch/swim neurons are general “multipurpose” limb motor control neurons while scratch-specialized neurons are quite specialized.

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