Downloads (link to download the article as PDF)
Download citations (links to download the citations from this article in formats compatible with various reference manager tools)
Open citations (links to open the citations from this article in various online reference manager services)
The CNS connectome of a tadpole larva of Ciona intestinalis (L.) highlights sidedness in the brain of a chordate sibling
- Dalhousie University, Canada
- Cited 15
- Views 1,904
Figures
Ultrathin section series of Ciona intestinalis larva, its CNS and notochord.
(A) Diagram of whole larva with colour-coded cell types indicated by arrows. Types of relay neurons (RNs) are shown as colour-coded territories in the brain vesicle. Muscle cells align in dorsal …
-
Figure 1—source data 1
Cell types: key to their characteristics and abbreviations used.
Includes colour key, defining features, subtypes, the numbers of neurons of each type, and a list of neurons of each type. Cells in bold correspond to bolded characteristics or subtypes.
- https://doi.org/10.7554/eLife.16962.005
Enlarged representative sections with labeled profiles from Figure 1B.
Sections presented for anterior brain vesicle (A), neck (B), anterior motor ganglion (C), posterior motor ganglion (D), and the caudal nerve cord (E), with profiles colour-coded by cell type (key) …
Synapses contain presynaptic vesicles of various sizes and types.
(A) Tightly packed cumulus of small (30–40 nm) vesicles at a single presynaptic site (arrow). (B) Mixed populations of small (30–50 nm) and large (70–110 nm) electron-lucent vesicles (arrow) as well …
-
Figure 2—source data 1
Neurons with synapses having mixed electron-lucent and dense-core vesicle populations (mixed), or exclusively dense-core vesicle (dcv) populations, with numbers (No.) of synapses of each type, and totals of both dcv and mixed vesicle synapses.
- https://doi.org/10.7554/eLife.16962.008
Synapse numbers (presynaptic sites) and sizes for all neurons (for complete list see Figure 3—source data 1).
(A) Most synaptic contacts extend over <10 60 nm sections. Those occupying >10 sections are neuromuscular junctions, inputs from relay neurons to MG neurons, and synapses from antenna cells. The …
-
Figure 3—source data 1
Summary of all neurons in the larval CNS of Ciona intestinalis.
Neurons listed by ID, with cell type, morphological features, location, presence or absence of cilia, and number of each neuron’s pre- and postsynaptic sites or putative gap junctions (>0.06 µm). Ependymal cells excluded. The final column shows left lateral views of individual neuron reconstructions (whole cells, or terminals for photoreceptors) as small thumbnails with scale bars: 1 µm (thick bars: coronet cells, lens cells, photoreceptor terminals and PR-III cells, vacINs); 10 µm (thin bars: all other cells).
- https://doi.org/10.7554/eLife.16962.010
Relationships between the morphology and synaptic output of larval CNS neurons.
(A) Number of synapses is not correlated with soma volume (μm3) (r2 = 0.4). (B) Soma volume does not correlate with the combined surface area of its axon and terminal regions (μm2) (r2 = 0.4). (C) …
Network graphs with network statistics visualized as attributes.
Edge-weighted spring embedded layout applied to both graphs, using EdgeBetweeness. (A) Network of chemical synapses. In-degree (number of presynaptic partners) mapped to node size, Out-degree …
Unpolarized, reciprocal, and serial synapses.
(A) Unpolarized mixed synapse between cell 115 and cell 23 with dense-core (arrowhead) and electron-lucent (arrow) vesicles on both sides of the synaptic cleft. (B) Single section with synapse from …
-
Figure 4—source data 1
Comparison of synaptic complements using different parameters and exclusion criteria.
Exclusions include synapses onto the basal lamina (bm), synapses onto ependymal cells (Ep), neuromuscular junctions (Mu), synapses onto no apparent postsynaptic neuron (space), and synapses observed in fewer than two sections (>1 section). For values excluding neuromuscular junctions the neuromuscular junction values and percentages are given.
- https://doi.org/10.7554/eLife.16962.014
Sensory neurons and associated cells have sided distributions.
Reconstructed coronet cells (Cor) with their bulbous protrusions (BP, one with a black arrow) and -- in their correct relative position -- six layers of photoreceptor neurons, excluding their …
Synapses of coronet cells.
(A) Synapse, containing exclusively dense-core vesicles (arrow), from a coronet cell onto the basal lamina (BL). (B) Unpolarized synapse between two coronet cells, with dense-core vesicles (arrows) …
Representation and relative sizes of cell bodies and their positions along the neuraxis, with corresponding axon tracts.
(A) Cell bodies of CNS neurons, dorsal view. Colours denote cell types (key). (B) Corresponding axon tracts, shown as skeleton reconstruction, dorsal view, colours as in (A) (for a network graph of …
Total network of synaptic pathways within the larval CNS of Ciona intestinalis.
Network graph of all connections within the larval nervous system generated in Cytoscape. Line width indicates synaptic strength (key, right) and arrows indicate direction of synaptic connection. …
Right-side interneurons reconstructed from the brain vesicle, left lateral views, anterior to the left.
(A) Intrinsic bipolar interneuron with two axons (arrows). (B) Anaxonal arborizing interneuron with large branched terminal (arrow). (C) Photoreceptor-ascending motor ganglion (pr-AMGRN) relay …
Asymmetrical sensory input to the two sides of the motor ganglion MG(L) and MG(R) via relay neurons.
Sensory input arises from coronet cells (Cor); antenna cells Ant1 and Ant2 (combined as Ant); and photoreceptors (PR) of two types: ocelli (oc: PR I) and neural canal (can: PR II). Signals are …
Total network of synaptic pathways within the larval CNS of Ciona intestinalis.
Network graph of all connections between cells of the larval nervous system grouped by cell type (cf, Figure 7—figure supplement 1). Line width indicates the total synaptic number (key, right) and …
Classes of relay neurons (presynaptic) in the CNS of Ciona and the inputs these provide to cells on the left and right sides of the motor ganglion (for details of relay inputs see Figure 10—figure supplement 1 and for antenna pathway see Figure 10—figure supplement 2).
For relay neuron class names see the key in Figure 1—source data 1). Each circle represents the input synapses to the first (column 1), second (column 2) or both (column 3) paired MG interneurons. …
-
Figure 10—source data 1
Relay neuron inputs to the left and right motor ganglion.
Values refer to the total number of synapses and their proportions of the whole population.
- https://doi.org/10.7554/eLife.16962.029
Reconstructions of motor ganglion neurons populated with photoreceptor and antenna relay neuron synaptic input sites, colour-coded by relay neuron type (key).
Synaptic sites are marked by 4 nm spheres regardless of their actual size. prRN: photoreceptor relay neuron; pr/trINRN: relay neurons with input from photoreceptors and photoreceptor tract …
Antenna cell relay neuron input to the motor ganglion.
(A) Network of antenna cell relay neuron synaptic connections to components of the motor ganglion. Cells are colour-coded, and synapse strength is denoted by line thicknesses (key, right) and varies …
The shortest CNS pathways between sensory neurons and motor neurons for different sensory modalities are three-synapse arcs.
Four modalities are indicated, from top to bottom: light, gravity, coronet cells (possibly hydrostatic pressure) and PNS mechano/chemosensory. Members of the same cell types are assigned the same …
Ciona intestinalis larval motor neuron terminals and neuromuscular junctions.
(A) Neuromuscular junction (arrow) of MN1, with a postsynaptic specialization on the muscle (arrowheads). A basal lamina (red arrow) extends in the cleft between neuron and muscle. (B) Two adjacent …
The networks of motor neurons MN1-MN5 and descending ipsilateral neurons (MG1-MG3) of the left and right side of the motor ganglion (MG).
(A) Synaptic network of motor neurons 1–5 on the left (MN1-5L) and right (MN1-5R) sides. (B) Network of putative gap junctions between motor neurons of the MG. (C) Summary diagrams of motor neuron …
Left-right asymmetries in the overall synaptic pathways of the motor ganglion.
Pathways shown are between motor neurons (MNs), descending ipsilateral interneurons (MGINs) and descending mid-tail neurons. (A) Synaptic network with arrows indicating polarity of synaptic …
ACIN synapses and network.
(A) Presynaptic site (arrow) from the left ACIN onto contralateral MGIN interneurons at a dyad synapse. BTN2: bipolar tail neuron profile. (B) Dyad synapse (arrow) onto ipsilateral motor neuron MN3R …
Entire connectivity matrix for the complete brain of a larva of Ciona intestinalis.
Shown for all synapses are the pre- (rows) and post- (columns) synaptic cells, colour-coded by cell type (see Figure 1—source data 1) and arranged in their rostro-caudal sequence along the …
-
Figure 16—source data 1
Matrix in Figure 16 1 as excel file.
- https://doi.org/10.7554/eLife.16962.040
-
Figure 16—source data 2
Matrix in Figure 16—figure supplement 2 as excel file.
- https://doi.org/10.7554/eLife.16962.041
Matrix of connections from Figure 16 sorted by left and right sides.
Cell types and connection strength are both coded by colour as in Figure 16 Rows and columns are sorted starting with cells connecting from left (L) to right (R), left to left, right to left and …
Entire matrix of putative gap junctions for the complete brain of a larva of Ciona intestinalis.
Shown for all neuron partners with a cumulative membrane contact depth of >0.12 µm, colour-coded by cell type and arranged in their rostro-caudal sequence along the longitudinal axis. Each intercept …
Videos
Symmetrical undulations of the tail in a swimming Ciona larva.
The tail lacks segmentation and in the 2 hr hatchling larva oscillates at 20–30 Hz at the juncture with the rostral trunk (Bone, 1992).
Rotation of reconstructed sensory structures.
Reconstructed pigment cells (black) with otolith associated ciliated cells (yellow) and vacuoles observed in a variety of cell types (lime green). Outer segments reconstructed as spheres for group I …
Rotation of reconstructed sensory neurons.
Reconstruction including transparent cell bodies illustrating pigment cells (black), group I (dark purple), group II (light purple) and group III (blue) photoreceptors with their outer segments …
Reconstruction of spheroids representing the cell body positions of sensory structures.
Pigment, photoreceptor and coronet cells with the bulbous protrusions (green) and photoreceptor outer segments (type I and type II: yellow; and type III: purple).
Rotations of reconstructed ACINs decorated with their presynaptic sites.
Reconstructed ACINs with presynaptic sites colour-coded by postsynaptic cell type: basal lamina (black); motor neuron (blue), descending MG interneuron (green), bipolar tail neuron (red), and …
Animated reconstruction of the photoreceptor pathway.
Cell bodies, shown as spheroids, from photoreceptor through relay neurons to the motor ganglion. Cells are colour-coded as in Figure 1—source data 1
Unilateral tail flick.
A larva exhibits a unilateral tail flick.
Asymmetrical tail flicks.
A larva exhibits repeated tail flicks to the same side of the trunk.
Tables
Numbers of synapses and gap junctions.
| Total no. | Total no. sections | Mean no. sections /contact | No. synapses> 1 section | Mean no. sections /contact >1 section | % Unpolarized | % Polyad | % Dcv | |
|---|---|---|---|---|---|---|---|---|
Synapses | 8617 | 30163 | 3.5 | 6618 | 4.3 | 5.2 | 10.7 | 8 |
Gap junctions | 3205 | 5765 | 1.8 | 1206 | 3.1 | ? | 3 | N/A |
-
Percentage (%) refers to the percentage of all synapses that are unpolarized (presynaptic vesicles on either side of the cleft between both neuron partners); polyadic (having >1 postsynaptic neurite); or containing dense-core vesicles (dcv) at the presynaptic site.
Network statistics for networks of chemical synapses and putative gap junctions.
Statistic | Synaptic network | Gap junction network | ||
|---|---|---|---|---|
Full network | CNS neurons only | Full network | CNS neurons only (>0.06 μm) | |
Clustering co-efficient | 0.333 | 0.335 | 0.25 | 0.305 |
Connected component | 1 | 1 | 7 | 1 |
Network diameter | 9 | 7 | 8 | 8 |
Radius | 1 | 4 | 1 | 4 |
Shortest paths | 90% [41001] | 95% [29759] | 85% [31536] | 100% [16770] |
Characteristic path length | 2.684 | 2.541 | 3.078 | 2.775 |
Average number of neighbours | 20.169 | 20.689 | 8.674 | 10.369 |
Number of nodes | 213 | 177 | 193 | 130 |
Network density | 0 | 0 | 0.045 | 0.08 |
Network heterogeneity | - | - | 0.935 | 0.76 |
Number of self-loops | 19 | 16 | 13 | 9 |
Multi-edge node pairs | 826 | 699 | 30 | 22 |
Network centralisation | - | - | 0.191 | 0.257 |
-
Network statistics calculated using the Cytoscape Network Analyzer for network of chemical synapses (Synaptic network) and putative gap junctions (Gap Junction network) for both the full network thus including PNS neurons, muscle, ambiguous cells, and synapses onto basal lamina, as well as CNS neurons; and the network for CNS neurons only (CNS neurons). Note that the 'CNS neurons only' network excludes one additional isolated profile of a single branch of one photoreceptor terminal, probably pr10.
Numbers of cells in the left, right and centre of the CNS and PNS.
Left | Centre | Right | |
|---|---|---|---|
Lens cells | 3 | ||
Pigment cells | 2 | ||
Total: Pigment and lens cells | 5 | ||
Coronet | 13* | 2 | 1 |
Photoreceptors | 37* | ||
Antenna neurons | 1 | 1 | |
Photoreceptor tract interneurons | 3* | ||
Anterior BV neurons | 29 | 1 | |
BV peripheral interneurons | 4 | 4 | 1 |
Bipolar neurons | 2 | ||
Anaxonal arborizing neurons | 1 | 2 | |
Posterior BV peripheral interneurons | 2 | 1 | 1 |
Photoreceptor relay neurons | 6 | ||
Photoreceptor-peripheral relay neurons | 2 | 2 | 6 |
Photoreceptor-coronet relay neurons | 2 | 1 | |
Antenna-coronet relay neuron | 1 | ||
Antenna relay neurons | 7 | 2 | |
Peripheral relay neurons | 2 | 1 | |
Relay interneurons | 5 | ||
Total: BV neurons | 72 | 14 | 57 |
Neck neurons | 1 | 1 | |
Total: Neck neurons | 1 | 1 | |
Ascending MG peripheral interneurons | 3 | 1 | 3 |
Descending decussating neurons | 1 | 1 | |
MG interneurons | 3 | 3 | |
Motor neurons | 5 | 5 | |
Total: MG neurons | 12 | 1 | 12 |
Ascending contralateral inhibitory neurons (ACINs) | 2 | 1 | |
Posterior MG interneurons | 2 | ||
Mid-tail neurons** | 2 | 2 | |
Total: CNC neurons | 4 | 5 | |
All CNS neurons | 88 | 15 | 75 |
Peripheral nervous system | |||
Bipolar tail neurons | 2 | 2 | |
Peripheral neurons (RTENa) | 6 | 6 | |
anterior ATENs | 2 | 2 | |
posterior ATENs | 4 | ||
DCENs | 4 | ||
Total: PNS neurons | 8 | 6 | 14 |
-
Neurons of the left side of the nervous system outnumber those of the right, which in turn outnumber those of the centre. All CNS neurons include known neurons that lack synapses (*).
-
**Additional mid-tail neurons which lay beyond the analysed region of the EM series are excluded from the totals.
Input to left and right dorsal and medial muscle bands from motor neuron pairs at their neuromuscular junctions.
Motor neuron pair | Left muscle band | Right muscle band | Ratios | |||||||
|---|---|---|---|---|---|---|---|---|---|---|
Dorsal | Medial | Dorsal | Medial | Left: Right | ||||||
No. syn | No. sec | No. syn | No. sec | No. syn | No. sec | No. syn | No. sec | No. syn | No. sec | |
MN1 | 192 | 969 | 47 | 145 | 230 | 1181 | 130 | 558 | 40: 60 | 39: 61 |
MN2 | 224 | 1583 | 258 | 1636 | 46: 54 | 49: 51 | ||||
MN3 | 42 | 156 | 28 | 101 | 60: 40 | 61: 39 | ||||
MN4 | 45 | 189 | 30 | 116 | 60: 40 | 62: 38 | ||||
MN5 | 21 | 128 | 15 | 55 | 58: 42 | 70: 30 | ||||
-
Number of synapses (No. syn) and number of synaptic profiles (No. sec) provided for each motor neuron and left:right ratios expressed as percentages of neuromuscular junction input from left and right partners for each motor neuron pair.
