Axon and dendrite geography predict the specificity of synaptic connections in a functioning spinal cord network

Li, Wen-Chang; Cooke, Tom; Sautois, Bart; Soffe, Stephen R; Borisyuk, Roman; Roberts, Alan

doi:10.1186/1749-8104-2-17

Cited by 54 publications

(79 citation statements)

References 57 publications

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“…The pattern of changes in firing from single to multiple spikes we observed during the development of zebrafish swimming was first described in Xenopus and most likely contributes to similar changes in their motor patterns (Sillar et al, 1992; Zhang et al, 2009). The recent description of dorso-ventral gradients in excitability and connectivity in Xenopus spinal cord suggest that a similar dorso-ventral pattern of function could be present in developing frogs (Li et al, 2007b; Pineda and Ribera, 2008). These similarities argue for the general applicability of our findings to developing swimming vertebrates, include a tetrapod ( Xenopus ).…”

Section: Discussionmentioning

confidence: 97%

Spinal Interneurons Differentiate Sequentially from Those Driving the Fastest Swimming Movements in Larval Zebrafish to Those Driving the Slowest Ones

McLean¹,

Fetcho²

2009

J. Neurosci.

149

161

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Studies of neuronal networks have revealed few general principles that link patterns of development with later functional roles. While investigating the neural control of movements, we recently discovered a topographic map in the spinal cord of larval zebrafish that relates the position of motoneurons and interneurons to their order of recruitment during swimming. Here, we show that the map reflects an orderly pattern of differentiation of neurons driving different movements. First, we use high-speed filming to show that large-amplitude swimming movements with bending along much of the body appear first, with smaller, regional swimming movements emerging later. Next, using whole-cell patch recordings, we demonstrate that the excitatory circuits that drive large-amplitude, fast swimming movements at larval stages are present and functional early on in embryos. Finally, we systematically assess the orderly emergence of spinal circuits according to swimming speed using transgenic fish expressing the photoconvertible protein Kaede to track neuronal differentiation in vivo. We conclude that a simple principle governs the development of spinal networks in which the neurons driving the fastest, most powerful swimming in larvae develop first with ones that drive increasingly weaker and slower larval movements layered on over time. Because the neurons are arranged by time of differentiation in the spinal cord, the result is a topographic map that represents the speed/strength of movements at which neurons are recruited and the temporal emergence of networks. This pattern may represent a general feature of neuronal network development throughout the brain and spinal cord.

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Section: Discussionmentioning

confidence: 97%

Spinal Interneurons Differentiate Sequentially from Those Driving the Fastest Swimming Movements in Larval Zebrafish to Those Driving the Slowest Ones

McLean¹,

Fetcho²

2009

J. Neurosci.

149

161

View full text Add to dashboard Cite

show abstract

“…At this level of neuron types, Peters’ rule has been applied in diverse species and neural systems, including the hatchling frog tadpole spinal cord [8], the cat primary visual cortex [9,10], the rodent hippocampus [11], and the mouse retina [12–15] and neocortex [16] as well as large-scale studies of the rat somatosensory cortex [17] and fly protocerebral bridge [18] (Table 1). The actual synaptic connectivity was in several cases found to corroborate the statistical impartiality of neuron types, thus quantitatively confirming Peters’ rule [9,15,19].…”

Section: Peters’ Rule: Original Intent and Promiscuous Generalizationsmentioning

confidence: 99%

Weighing the Evidence in Peters’ Rule: Does Neuronal Morphology Predict Connectivity?

Rees

Moradi

Ascoli

2017

Trends in Neurosciences

112

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Although the importance of network connectivity is increasingly recognized, identifying synapses remains challenging relative to the routine characterization of neuronal morphology. Thus, researchers frequently employ axon–dendrite colocations as proxies of potential connections. This putative equivalence, commonly referred to as Peters’ rule, has been recently studied at multiple levels and scales, fueling passionate debates regarding its validity. Our critical literature review identifies three conceptually distinct but often confused applications: inferring neuron type circuitry, predicting synaptic contacts among individual cells, and estimating synapse numbers within neuron pairs. Paradoxically, at the originally proposed cell-type level, Peters’ rule remains largely untested. Leveraging Hippocampome.org, we validate and refine the relationship between axonal–dendritic colocations and synaptic circuits, clarifying the interpretation of existing and forthcoming data.

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“…It also poses questions about the rules of specificity that govern the assembly of inhibitory circuits. Suggestions that GABAergic neurons seek out synaptic partners with high precision (Thomson and Morris, 2002; Stepanyants et al, 2004) have been countered by proposals that inhibitory networks can assemble in the absence of specificity cues (Li et al, 2007). …”

Section: Introductionmentioning

confidence: 99%

Stringent Specificity in the Construction of a GABAergic Presynaptic Inhibitory Circuit

Betley

Wright

Kawaguchi

et al. 2009

Cell

194

274

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Summary GABAergic interneurons are key elements in neural coding, but the mechanisms that assemble inhibitory circuits remain unclear. In the spinal cord, the transfer of sensory signals to motor neurons is filtered by GABAergic interneurons that act pre-synaptically to inhibit sensory transmitter release and post-synaptically to inhibit motor neuron excitability. We show here that the connectivity and synaptic differentiation of GABAergic interneurons that mediate pre-synaptic inhibition is directed by their sensory targets. In the absence of sensory terminals these GABAergic neurons shun other available targets, fail to undergo pre-synaptic differentiation, and withdraw axons from the ventral spinal cord. A sensory-specific source of brain derived neurotrophic factor induces synaptic expression of the GABA synthetic enzyme GAD65 – a defining biochemical feature of this set of interneurons. The organization of a GABAergic circuit that mediates pre-synaptic inhibition in the mammalian CNS is therefore controlled by a stringent program of sensory recognition and signaling.

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Axon and dendrite geography predict the specificity of synaptic connections in a functioning spinal cord network

Cited by 54 publications

References 57 publications

Spinal Interneurons Differentiate Sequentially from Those Driving the Fastest Swimming Movements in Larval Zebrafish to Those Driving the Slowest Ones

Spinal Interneurons Differentiate Sequentially from Those Driving the Fastest Swimming Movements in Larval Zebrafish to Those Driving the Slowest Ones

Weighing the Evidence in Peters’ Rule: Does Neuronal Morphology Predict Connectivity?

Stringent Specificity in the Construction of a GABAergic Presynaptic Inhibitory Circuit

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