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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

Activity of specialized excitatory sensory pathway interneurons in the tadpole. (A) A dlc fires once, following a brief skin stimulus to the same side (▼). It does not fire during subsequent swimming, seen as rhythmic activity at a ventral root and in a cIN recorded simultaneously on the same side. (B) An ecIN does not fire during swimming but is recruited by summating excitation (*) during 40-Hz skin stimulation to fire strongly during struggling. An inhibitory premotor cIN recorded at the same time is also recruited during struggling, but, unlike the ecIN, fires strongly from the start of skin stimulation.
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Figure 8: Activity of specialized excitatory sensory pathway interneurons in the tadpole. (A) A dlc fires once, following a brief skin stimulus to the same side (▼). It does not fire during subsequent swimming, seen as rhythmic activity at a ventral root and in a cIN recorded simultaneously on the same side. (B) An ecIN does not fire during swimming but is recruited by summating excitation (*) during 40-Hz skin stimulation to fire strongly during struggling. An inhibitory premotor cIN recorded at the same time is also recruited during struggling, but, unlike the ecIN, fires strongly from the start of skin stimulation.

Mentions: Two types of sensory pathway interneurons relay information about brief touch of the trunk skin from the primary sensory Rohon-Beard neurons. The dorsolateral commissural (dlc) and dorsolateral ascending (dla) interneurons have axons projecting rostrally into the hindbrain on the opposite side and the same side, respectively (Roberts and Clarke, 1982; Roberts and Sillar, 1990; Li et al., 2001, 2003, 2004b). The contralateral axons of dlcs also often branch to descend. These dlc and dla sensory pathway interneurons share several features: their characteristic dorsolateral position in the cord, their adapting firing properties, their very strong, fast, glutamatergic excitation by Rohon-Beard neurons, and their weaker, glutamatergic excitation of motoneurons and premotor interneurons, which relies on summation of input from several pre-synaptic neurons to be effective (Li et al., 2003, 2004b). Following a brief stimulus to the trunk skin, dlcs and dlas can each quickly fire a single spike (Figure 8A). The result of the stimulus is usually a reflex motor response (flexion reflex) on the opposite side. The mechanism favoring a contralateral rather than ipsilateral response has been investigated, but remains unclear (Zhao et al., 1998). In addition to their role in flexion reflexes, dlcs and dlas are involved in the initiation of swimming (ultimately producing self-sustaining firing in members of the excitatory dIN population in the caudal hindbrain and rostral spinal cord (Soffe, 1993; Li et al., 2004a, 2006)). Both are inactive during swimming itself since they are subject to rhythmic inhibition from aINs. During struggling, strong recruitment of aIN firing and the consequent summation of this aIN inhibition prevents dlcs and dlas from firing (Soffe, 1993). The dlc and dla sensory pathway interneurons are therefore specialized for mediating flexion reflex responses and the initiation of swimming in response to brief touch.


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)

Activity of specialized excitatory sensory pathway interneurons in the tadpole. (A) A dlc fires once, following a brief skin stimulus to the same side (▼). It does not fire during subsequent swimming, seen as rhythmic activity at a ventral root and in a cIN recorded simultaneously on the same side. (B) An ecIN does not fire during swimming but is recruited by summating excitation (*) during 40-Hz skin stimulation to fire strongly during struggling. An inhibitory premotor cIN recorded at the same time is also recruited during struggling, but, unlike the ecIN, fires strongly from the start of skin stimulation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Activity of specialized excitatory sensory pathway interneurons in the tadpole. (A) A dlc fires once, following a brief skin stimulus to the same side (▼). It does not fire during subsequent swimming, seen as rhythmic activity at a ventral root and in a cIN recorded simultaneously on the same side. (B) An ecIN does not fire during swimming but is recruited by summating excitation (*) during 40-Hz skin stimulation to fire strongly during struggling. An inhibitory premotor cIN recorded at the same time is also recruited during struggling, but, unlike the ecIN, fires strongly from the start of skin stimulation.
Mentions: Two types of sensory pathway interneurons relay information about brief touch of the trunk skin from the primary sensory Rohon-Beard neurons. The dorsolateral commissural (dlc) and dorsolateral ascending (dla) interneurons have axons projecting rostrally into the hindbrain on the opposite side and the same side, respectively (Roberts and Clarke, 1982; Roberts and Sillar, 1990; Li et al., 2001, 2003, 2004b). The contralateral axons of dlcs also often branch to descend. These dlc and dla sensory pathway interneurons share several features: their characteristic dorsolateral position in the cord, their adapting firing properties, their very strong, fast, glutamatergic excitation by Rohon-Beard neurons, and their weaker, glutamatergic excitation of motoneurons and premotor interneurons, which relies on summation of input from several pre-synaptic neurons to be effective (Li et al., 2003, 2004b). Following a brief stimulus to the trunk skin, dlcs and dlas can each quickly fire a single spike (Figure 8A). The result of the stimulus is usually a reflex motor response (flexion reflex) on the opposite side. The mechanism favoring a contralateral rather than ipsilateral response has been investigated, but remains unclear (Zhao et al., 1998). In addition to their role in flexion reflexes, dlcs and dlas are involved in the initiation of swimming (ultimately producing self-sustaining firing in members of the excitatory dIN population in the caudal hindbrain and rostral spinal cord (Soffe, 1993; Li et al., 2004a, 2006)). Both are inactive during swimming itself since they are subject to rhythmic inhibition from aINs. During struggling, strong recruitment of aIN firing and the consequent summation of this aIN inhibition prevents dlcs and dlas from firing (Soffe, 1993). The dlc and dla sensory pathway interneurons are therefore specialized for mediating flexion reflex responses and the initiation of swimming in response to brief touch.

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