Limits...
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

The struggling motor pattern, the neurons responsible and its mechanism of generation. (A,B) During 40-Hz skin stimuli struggling is evoked and a cIN and ecIN recorded in whole-cell mode are recruited. When stimulation stops the motor pattern switches to swimming and recorded neurons become silent. (C) Current injection into the ecIN makes it fire an action potential which produces a short latency EPSP in the cIN. (D) Longer injected current induces typical repetitive firing. (E) Measures of 1st and 10th compound IPSCs evoked in a dIN by stimulation of the opposite side show significant depression only with 100-Hz stimulation. (F) Half-center model of struggling network without length with three of each type of neuron on each side. (G) If cIN inhibition shows depression, this network can reliably generate struggling- like activity during tonic sensory excitation. (based on Li et al., 2007).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2903309&req=5

Figure 6: The struggling motor pattern, the neurons responsible and its mechanism of generation. (A,B) During 40-Hz skin stimuli struggling is evoked and a cIN and ecIN recorded in whole-cell mode are recruited. When stimulation stops the motor pattern switches to swimming and recorded neurons become silent. (C) Current injection into the ecIN makes it fire an action potential which produces a short latency EPSP in the cIN. (D) Longer injected current induces typical repetitive firing. (E) Measures of 1st and 10th compound IPSCs evoked in a dIN by stimulation of the opposite side show significant depression only with 100-Hz stimulation. (F) Half-center model of struggling network without length with three of each type of neuron on each side. (G) If cIN inhibition shows depression, this network can reliably generate struggling- like activity during tonic sensory excitation. (based on Li et al., 2007).

Mentions: The main spinal neuron types, their activity during swimming and their synaptic connections have now been defined and proposals about how the spinal swimming circuits work tested using model networks (review Roberts, 1990). In the hatchling tadpole, though not at later stages (Sillar et al., 1991; McLean et al., 2000b), most spinal interneurons and motoneurons which are active during swimming: fire a single spike at a similar phase to motoneurons on each cycle, receive mid-cycle inhibition, and do not spike at rest (Figure 3B). The exception is ascending interneurons (aINs) which produce glycinergic recurrent inhibition to limit motoneuron firing and can fire more than once on each cycle (Li et al., 2004a). The glycinergic neurons producing mid-cycle reciprocal inhibition are commissural interneurons (cINs; Dale, 1985). Initially the identity of the excitatory descending interneurons (dINs) was rather uncertain but dramatically, they produced long duration glutamate excitation mediated by the activation of NMDA receptors (Dale and Roberts, 1985). In 0 Mg2+ saline, this excitation could sum at swimming frequencies to produce an activity dependent tonic excitation. Sharp microelectrode recordings with marker filling also revealed that reticulospinal neurons, resembling dINs morphologically, were rhythmically active and fired once on each cycle of swimming (van Mier and ten Donkelaar, 1989). Recent whole-cell recording with neurobiotin injection to obtain anatomy has been most significant in confirming the role of dINs as the source of the excitatory drive for swimming locomotion (Li et al., 2006), something that has proven so difficult to track down in mammals (Kiehn, 2006). There is now direct evidence on the properties and connections of dINs. They have an unusually long-duration action potential compared to all other neurons active during swimming (Figure 3B) and usually only fire a single action potential to depolarizing current even well above threshold (Figure 3D). This contrasts with other spinal neurons which fire repetitively to injected current (eg Figure 6D). By recording from many pairs of connected neurons ample direct evidence is now available that dINs produce mainly fast excitation of cINs, aINs and mns (eg Figure 3C). Remarkably, they do this by co-releasing glutamate and acetylcholine which activates AMPA and nicotinic acetylcholine receptors (Li et al., 2004c). Another discovery was also interesting. When dINs in the hindbrain were filled with neurobiotin, a much higher proportion had additional ascending axons and these allowed them to make reciprocal excitatory synapses (Figure 3F). At last we had direct evidence for the proposed NMDAR mediated feedback excitation (Dale and Roberts, 1985). The final important property of dINs is that they show post-inhibitory rebound firing to negative current pulses and IPSPs when they are depolarized (Figure 3E; Soffe et al., 2009) but IPSPs and negative current injection at rest rarely lead to delayed rebound firing as they do in the interneurons driving swimming in the marine mollusc Clione (Satterlie, 1985).


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

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

The struggling motor pattern, the neurons responsible and its mechanism of generation. (A,B) During 40-Hz skin stimuli struggling is evoked and a cIN and ecIN recorded in whole-cell mode are recruited. When stimulation stops the motor pattern switches to swimming and recorded neurons become silent. (C) Current injection into the ecIN makes it fire an action potential which produces a short latency EPSP in the cIN. (D) Longer injected current induces typical repetitive firing. (E) Measures of 1st and 10th compound IPSCs evoked in a dIN by stimulation of the opposite side show significant depression only with 100-Hz stimulation. (F) Half-center model of struggling network without length with three of each type of neuron on each side. (G) If cIN inhibition shows depression, this network can reliably generate struggling- like activity during tonic sensory excitation. (based on Li et al., 2007).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: The struggling motor pattern, the neurons responsible and its mechanism of generation. (A,B) During 40-Hz skin stimuli struggling is evoked and a cIN and ecIN recorded in whole-cell mode are recruited. When stimulation stops the motor pattern switches to swimming and recorded neurons become silent. (C) Current injection into the ecIN makes it fire an action potential which produces a short latency EPSP in the cIN. (D) Longer injected current induces typical repetitive firing. (E) Measures of 1st and 10th compound IPSCs evoked in a dIN by stimulation of the opposite side show significant depression only with 100-Hz stimulation. (F) Half-center model of struggling network without length with three of each type of neuron on each side. (G) If cIN inhibition shows depression, this network can reliably generate struggling- like activity during tonic sensory excitation. (based on Li et al., 2007).
Mentions: The main spinal neuron types, their activity during swimming and their synaptic connections have now been defined and proposals about how the spinal swimming circuits work tested using model networks (review Roberts, 1990). In the hatchling tadpole, though not at later stages (Sillar et al., 1991; McLean et al., 2000b), most spinal interneurons and motoneurons which are active during swimming: fire a single spike at a similar phase to motoneurons on each cycle, receive mid-cycle inhibition, and do not spike at rest (Figure 3B). The exception is ascending interneurons (aINs) which produce glycinergic recurrent inhibition to limit motoneuron firing and can fire more than once on each cycle (Li et al., 2004a). The glycinergic neurons producing mid-cycle reciprocal inhibition are commissural interneurons (cINs; Dale, 1985). Initially the identity of the excitatory descending interneurons (dINs) was rather uncertain but dramatically, they produced long duration glutamate excitation mediated by the activation of NMDA receptors (Dale and Roberts, 1985). In 0 Mg2+ saline, this excitation could sum at swimming frequencies to produce an activity dependent tonic excitation. Sharp microelectrode recordings with marker filling also revealed that reticulospinal neurons, resembling dINs morphologically, were rhythmically active and fired once on each cycle of swimming (van Mier and ten Donkelaar, 1989). Recent whole-cell recording with neurobiotin injection to obtain anatomy has been most significant in confirming the role of dINs as the source of the excitatory drive for swimming locomotion (Li et al., 2006), something that has proven so difficult to track down in mammals (Kiehn, 2006). There is now direct evidence on the properties and connections of dINs. They have an unusually long-duration action potential compared to all other neurons active during swimming (Figure 3B) and usually only fire a single action potential to depolarizing current even well above threshold (Figure 3D). This contrasts with other spinal neurons which fire repetitively to injected current (eg Figure 6D). By recording from many pairs of connected neurons ample direct evidence is now available that dINs produce mainly fast excitation of cINs, aINs and mns (eg Figure 3C). Remarkably, they do this by co-releasing glutamate and acetylcholine which activates AMPA and nicotinic acetylcholine receptors (Li et al., 2004c). Another discovery was also interesting. When dINs in the hindbrain were filled with neurobiotin, a much higher proportion had additional ascending axons and these allowed them to make reciprocal excitatory synapses (Figure 3F). At last we had direct evidence for the proposed NMDAR mediated feedback excitation (Dale and Roberts, 1985). The final important property of dINs is that they show post-inhibitory rebound firing to negative current pulses and IPSPs when they are depolarized (Figure 3E; Soffe et al., 2009) but IPSPs and negative current injection at rest rarely lead to delayed rebound firing as they do in the interneurons driving swimming in the marine mollusc Clione (Satterlie, 1985).

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