Initiation of Locomotion in Adult Zebrafish

Kyriakatos, Alexandros; Mahmood, Riyadh; Ausborn, Jessica; Porres, Christian P.; Büschges, Ansgar; Manira, Abdeljabbar El

doi:10.1523/jneurosci.1012-11.2011

Cited by 79 publications

(71 citation statements)

References 62 publications

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“…Selective innervation by nociceptive Trpa1b afferents suggests that there might be functional similarity between fish and mammals in this anatomical region. The identities and function of Trpa1b target cells are not yet known, but this region has recently been proposed to contain specialized cells that can initiate persistent swimming (Kyriakatos et al, 2011). This would be consistent with the observation that Trpa1b activation increases overall motor activity and raises the possibility that Isl1SS and Trpa1b subtypes have distinct abilities to trigger persistent swimming.…”

Section: Functional Implications Of Subtype-specific Projection Patternssupporting

confidence: 74%

Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons

et al. 2012

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SUMMARYHow neurons connect to form functional circuits is central to the understanding of the development and function of the nervous system. In the somatosensory system, perception of sensory stimuli to the head requires specific connections between trigeminal sensory neurons and their many target areas in the central nervous system. Different trigeminal subtypes have specialized functions and downstream circuits, but it has remained unclear how subtype-specific axonal projection patterns are formed. Using zebrafish as a model system, we followed the development of two trigeminal sensory neuron subtypes: one that expresses trpa1b, a nociceptive channel important for sensing environmental chemicals; and a distinct subtype labeled by an islet1 reporter (Isl1SS). We found that Trpa1b and Isl1SS neurons have overall similar axon trajectories but different branching morphologies and distributions of presynaptic sites. Compared with Trpa1b neurons, Isl1SS neurons display reduced branch growth and synaptogenesis at the hindbrain-spinal cord junction. The subtype-specific morphogenesis of Isl1SS neurons depends on the guidance receptor Robo2. robo2 is preferentially expressed in the Isl1SS subset and inhibits branch growth and synaptogenesis. In the absence of Robo2, Isl1SS afferents acquire many of the characteristics of Trpa1b afferents. These results reveal that subtypespecific activity of Robo2 regulates subcircuit morphogenesis in the trigeminal sensory system.

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Section: Functional Implications Of Subtype-specific Projection Patternssupporting

confidence: 74%

Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons

et al. 2012

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“…2F). These results show that different subsets of V2a interneurons are recruited incrementally to cover swimming frequencies between 1 and 10 Hz, a range that represents 70% of the frequencies at which intact juvenile/adult zebrafish swim (37).…”

Section: Resultsmentioning

confidence: 77%

“…Swimming activity was induced by electrical stimulation of descending axons in an in vitro brainstem-spinal cord preparation and was monitored by recording from a peripheral motor nerve (Fig. 1B) (37). V2a interneurons were recorded at different dorsoventral and lateromedial positions using patch-clamp techniques ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Our results suggest that mechanisms underlying the recruitment of neurons in the spinal cord may undergo a refinement as the zebrafish develop toward adulthood. This refinement could be reflected in a reconfiguration of the organization of the swimming circuits to accommodate the changes in the swimming pattern and frequency range between early and adult developmental stages (10,30,36,37,(42)(43)(44)(45). It is not yet clear whether the scrambling of the topographic order of V2a interneuron recruitment mirrors only the displacement of these interneurons, an additional tuning of their cellular and synaptic features, or both.…”

Section: Mechanisms Defining the Recruitment Threshold Of V2a Internementioning

confidence: 99%

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Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network

Ausborn

Mahmood

Manira

2012

Proc. Natl. Acad. Sci. U.S.A.

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Neural networks in the spinal cord transform signals from the brain into coordinated locomotor movements. An optimal adjustment of the speed of locomotion entails a precise order of recruitment of interneurons underlying excitation within these networks. However, the mechanisms encoding the recruitment threshold of excitatory interneurons have remained unclear. Here we show, using a juvenile/adult zebrafish preparation, that excitatory V2a interneurons are incrementally recruited with increased swimming frequency. The order of recruitment is not imprinted by the topography or the input resistance of the V2a interneurons. Rather, it is determined by scaling the effect of excitatory synaptic currents by the input resistance. We also show that the locomotor networks are composed of multiple microcircuits encompassing subsets of V2a interneurons and motoneurons that are recruited in a continuum with increased swimming speeds. Thus, our results provide insights into the organization and mechanisms determining the recruitment of spinal microcircuits to ensure optimal execution of locomotor movements.central pattern generator | synaptic transmission | Chx10 N eural networks in the spinal cord generate locomotion and serve in a variety of behavioral contexts (1-7). They undergo continuous adjustments to accommodate the contextual demands to produce locomotor movements with appropriate speed, force, and timing. An appreciable understanding of the molecular logic of the assembly of spinal circuits at early developmental stages has begun to emerge (8-21). However, the mechanisms underlying speed control of locomotor movements have remained unclear.Changing locomotor speed ultimately involves a sequential activation of different motoneurons that represent the final stage of processing in the spinal cord (22-24). However, motoneurons are not primarily involved in the generation of the locomotor rhythm, a task undertaken by premotor interneurons. V2a interneurons are a neuronal class of critical importance to the vertebrate locomotor network (1,8,12,15,(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35). Partial ablation of these interneurons in zebrafish decreases the excitability of the spinal networks (30). Thus, changes in the speed of locomotor movements would be initiated at the level of V2a interneurons that set the excitatory tone within the locomotor networks. The pattern of activation of V2a interneurons during locomotion has been examined in zebrafish larvae and embryos and in newborn mice (15,32,36). However, the mechanisms defining the recruitment threshold of V2a interneurons as a function of locomotor frequency have remained obscure.We have investigated how V2a interneurons are recruited at different swimming speeds in the juvenile/adult zebrafish. Our findings show that although the excitatory drive of V2a interneurons is graded topographically, their order of recruitment does not obey a topographic map. Rather their recruitment threshold is set by a scaling of the excitatory drive by the input resistance that result...

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“…The spinal cord acts as an interface to process descending commands from the brain and sensory inputs from the periphery (5,8,(10)(11)(12)(13)(14)(15)(16). Many insights into the organization and function of circuits underlying motor behavior have been gained from studies of spinal networks controlling locomotor movements (6,13,(17)(18)(19)(20)(21)(22)(23)(24).…”

mentioning

confidence: 99%

Origin of excitation underlying locomotion in the spinal circuit of zebrafish

Eklöf-Ljunggren

Haupt²,

Ausborn³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Neural circuits in the spinal cord transform instructive signals from the brain into well-coordinated locomotor movements by virtue of rhythm-generating components. Although evidence suggests that excitatory interneurons are the essence of locomotor rhythm generation, their molecular identity and the assessment of their necessity have remained unclear. Here we show, using larval zebrafish, that V2a interneurons represent an intrinsic source of excitation necessary for the normal expression of the locomotor rhythm. Acute and selective ablation of these interneurons increases the threshold of induction of swimming activity, decreases the burst frequency, and alters the coordination of the rostro-caudal propagation of activity. Thus, our results argue that V2a interneurons represent a source of excitation that endows the spinal circuit with the capacity to generate locomotion.central pattern generator | premotor interneurons | motor behavior | synaptic transmission T he generation of motor behavior involves decision making, selection, initiation, and execution (1-9). The spinal cord acts as an interface to process descending commands from the brain and sensory inputs from the periphery (5,8,(10)(11)(12)(13)(14)(15)(16). Many insights into the organization and function of circuits underlying motor behavior have been gained from studies of spinal networks controlling locomotor movements (6,13,(17)(18)(19)(20)(21)(22)(23)(24). The basic locomotor activity requires the interplay of ipsilateral excitatory drive and crossed inhibition, which ensures the alternating pattern between the two sides of the spinal cord. Whereas inhibitory interneurons ensure the coordination of motoneurons controlling antagonistic muscles, excitatory interneurons are believed to represent the core components for the generation of the locomotor rhythm.Determining the identity of the interneurons at the origin of excitation necessary for the normal generation of locomotor activity is central for understanding the principles of organization and function of locomotor circuits. However, the molecular identity of these excitatory interneurons has remained unclear. A prominent class of excitatory interneurons is the V2a interneurons, defined by Chx10 expression and derived from the p2 progenitor domain with homologous counterparts across vertebrate species (21,(25)(26)(27). In larval zebrafish and newborn mice, V2a interneurons have been shown to project to motoneurons and to be recruited in a frequency-dependent manner (28-32). These properties are consistent with the possibility that this class of interneurons represents a source of excitation within the spinal locomotor circuit.In newborn mice, however, genetic elimination of V2a interneurons has been reported to have little effect on the rhythmic output of the locomotor circuits induced by pharmacological means (33, 34). The absence of tangible effects on the excitability of the locomotor circuit in the absence of V2a interneurons led to the conclusion that these interneurons are not essential fo...

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Initiation of Locomotion in Adult Zebrafish

Cited by 79 publications

References 62 publications

Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons

Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons

Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network

Origin of excitation underlying locomotion in the spinal circuit of zebrafish

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