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How neurons generate behavior in a hatchling amphibian tadpole: an outline.

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

Bottom Line: We then examine GABAergic inhibitory pathways that control swimming but also produce tonic inhibition to reduce responsiveness when the tadpole is at rest.We show that the mechanisms for rhythm generation here are very different to those during swimming.Although much remains to be explained, study of this simple vertebrate has uncovered basic principles about the function and organization of vertebrate nervous systems.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, University of Bristol , Bristol, UK.

ABSTRACT
Adult nervous systems are so complex that understanding how they produce behavior remains a real challenge. We chose to study hatchling Xenopus tadpoles where behavior is controlled by a few thousand neurons but there is a very limited number of types of neuron. Young tadpoles can flex, swim away, adjust their trajectory, speed-up and slow-down, stop when they contact support and struggle when grasped. They are sensitive to touch, pressure, noxious stimuli, light intensity and water currents. Using whole-cell recording has led to rapid progress in understanding central networks controlling behavior. Our methods are illustrated by an analysis of the flexion reflex to skin touch. We then define the seven types of neuron that allow the tadpole to swim when the skin is touched and use paired recordings to investigate neuron properties, synaptic connections and activity patterns. Proposals on how the swim network operates are evaluated by experiment and network modeling. We then examine GABAergic inhibitory pathways that control swimming but also produce tonic inhibition to reduce responsiveness when the tadpole is at rest. Finally, we analyze the strong alternating struggling movements the tadpole makes when grasped. We show that the mechanisms for rhythm generation here are very different to those during swimming. Although much remains to be explained, study of this simple vertebrate has uncovered basic principles about the function and organization of vertebrate nervous systems.

No MeSH data available.


Related in: MedlinePlus

Swimming: effects of lesions, activity patterns and excitation. (A) CNS in dorsal view to show suction electrode positions to record alternating ventral root (vr) spikes during swimming generated by an isolated 0.3-mm long region of CNS (gray). (B) Whole-cell recording from a cIN and hindbrain dIN (hdIN) show both fire once on each cycle of swimming and the hdIN has a long action potential; (C) spike evoked in the hdIN by current (arrowhead) leads to an EPSP in the cIN. (D) A dIN fires once to positive current but does not fire on rebound after negative current. (E) If large enough, negative current pulses during depolarization can lead to post-inhibitory rebound firing. (F) Recording from a pair of dINs in the hindbrain shows that when current is injected to make them fire (arrowheads) they produce long duration excitation in the other. (based on Li et al., 2006).
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Figure 3: Swimming: effects of lesions, activity patterns and excitation. (A) CNS in dorsal view to show suction electrode positions to record alternating ventral root (vr) spikes during swimming generated by an isolated 0.3-mm long region of CNS (gray). (B) Whole-cell recording from a cIN and hindbrain dIN (hdIN) show both fire once on each cycle of swimming and the hdIN has a long action potential; (C) spike evoked in the hdIN by current (arrowhead) leads to an EPSP in the cIN. (D) A dIN fires once to positive current but does not fire on rebound after negative current. (E) If large enough, negative current pulses during depolarization can lead to post-inhibitory rebound firing. (F) Recording from a pair of dINs in the hindbrain shows that when current is injected to make them fire (arrowheads) they produce long duration excitation in the other. (based on Li et al., 2006).

Mentions: The most obvious behavior of newly hatched fish and amphibians is swimming. Our investigation of the tadpole swimming network raises questions about the generally accepted hypothesis that spinal cord networks called central pattern generators, organized as half-centers, produce a rhythmic locomotor pattern if provided with steady, unpatterned excitation by the brain (Orlovsky et al., 1999). The fact that a swimming-like pattern of motor nerve activity alternating on the left and right and progressing from head to tail can occur in response to brief skin stimulation in immobilized fish and amphibian larvae shows that the basic swimming pattern can be generated without reflexes by the CNS (Kahn and Roberts, 1982a; Drapeau et al., 2002). Lesions in Xenopus tadpoles show that the basic pattern can still be generated for many seconds after a brief stimulus by a 0.3-mm long region of caudal hindbrain and rostral spinal cord (Figure 3A; Li et al., 2006). This small region of CNS must therefore contain sufficient neurons and connections to generate a self-sustained basic swimming rhythm. On the other hand, the spinal cord alone can only generate a few cycles of rhythm following a skin stimulus. However, as in other decerebrated animals (Stein et al., 1997), if artificial excitation is provided by bath application of NMDA, then the spinal cord can organise long lasting swimming-like activity (Li et al., 2006). There are therefore two main things to explain: how does the nervous system sustain locomotor activity after it is initiated and, how is the pattern of motor output organized?


How neurons generate behavior in a hatchling amphibian tadpole: an outline.

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

Swimming: effects of lesions, activity patterns and excitation. (A) CNS in dorsal view to show suction electrode positions to record alternating ventral root (vr) spikes during swimming generated by an isolated 0.3-mm long region of CNS (gray). (B) Whole-cell recording from a cIN and hindbrain dIN (hdIN) show both fire once on each cycle of swimming and the hdIN has a long action potential; (C) spike evoked in the hdIN by current (arrowhead) leads to an EPSP in the cIN. (D) A dIN fires once to positive current but does not fire on rebound after negative current. (E) If large enough, negative current pulses during depolarization can lead to post-inhibitory rebound firing. (F) Recording from a pair of dINs in the hindbrain shows that when current is injected to make them fire (arrowheads) they produce long duration excitation in the other. (based on Li et al., 2006).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2903309&req=5

Figure 3: Swimming: effects of lesions, activity patterns and excitation. (A) CNS in dorsal view to show suction electrode positions to record alternating ventral root (vr) spikes during swimming generated by an isolated 0.3-mm long region of CNS (gray). (B) Whole-cell recording from a cIN and hindbrain dIN (hdIN) show both fire once on each cycle of swimming and the hdIN has a long action potential; (C) spike evoked in the hdIN by current (arrowhead) leads to an EPSP in the cIN. (D) A dIN fires once to positive current but does not fire on rebound after negative current. (E) If large enough, negative current pulses during depolarization can lead to post-inhibitory rebound firing. (F) Recording from a pair of dINs in the hindbrain shows that when current is injected to make them fire (arrowheads) they produce long duration excitation in the other. (based on Li et al., 2006).
Mentions: The most obvious behavior of newly hatched fish and amphibians is swimming. Our investigation of the tadpole swimming network raises questions about the generally accepted hypothesis that spinal cord networks called central pattern generators, organized as half-centers, produce a rhythmic locomotor pattern if provided with steady, unpatterned excitation by the brain (Orlovsky et al., 1999). The fact that a swimming-like pattern of motor nerve activity alternating on the left and right and progressing from head to tail can occur in response to brief skin stimulation in immobilized fish and amphibian larvae shows that the basic swimming pattern can be generated without reflexes by the CNS (Kahn and Roberts, 1982a; Drapeau et al., 2002). Lesions in Xenopus tadpoles show that the basic pattern can still be generated for many seconds after a brief stimulus by a 0.3-mm long region of caudal hindbrain and rostral spinal cord (Figure 3A; Li et al., 2006). This small region of CNS must therefore contain sufficient neurons and connections to generate a self-sustained basic swimming rhythm. On the other hand, the spinal cord alone can only generate a few cycles of rhythm following a skin stimulus. However, as in other decerebrated animals (Stein et al., 1997), if artificial excitation is provided by bath application of NMDA, then the spinal cord can organise long lasting swimming-like activity (Li et al., 2006). There are therefore two main things to explain: how does the nervous system sustain locomotor activity after it is initiated and, how is the pattern of motor output organized?

Bottom Line: We then examine GABAergic inhibitory pathways that control swimming but also produce tonic inhibition to reduce responsiveness when the tadpole is at rest.We show that the mechanisms for rhythm generation here are very different to those during swimming.Although much remains to be explained, study of this simple vertebrate has uncovered basic principles about the function and organization of vertebrate nervous systems.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, University of Bristol , Bristol, UK.

ABSTRACT
Adult nervous systems are so complex that understanding how they produce behavior remains a real challenge. We chose to study hatchling Xenopus tadpoles where behavior is controlled by a few thousand neurons but there is a very limited number of types of neuron. Young tadpoles can flex, swim away, adjust their trajectory, speed-up and slow-down, stop when they contact support and struggle when grasped. They are sensitive to touch, pressure, noxious stimuli, light intensity and water currents. Using whole-cell recording has led to rapid progress in understanding central networks controlling behavior. Our methods are illustrated by an analysis of the flexion reflex to skin touch. We then define the seven types of neuron that allow the tadpole to swim when the skin is touched and use paired recordings to investigate neuron properties, synaptic connections and activity patterns. Proposals on how the swim network operates are evaluated by experiment and network modeling. We then examine GABAergic inhibitory pathways that control swimming but also produce tonic inhibition to reduce responsiveness when the tadpole is at rest. Finally, we analyze the strong alternating struggling movements the tadpole makes when grasped. We show that the mechanisms for rhythm generation here are very different to those during swimming. Although much remains to be explained, study of this simple vertebrate has uncovered basic principles about the function and organization of vertebrate nervous systems.

No MeSH data available.


Related in: MedlinePlus