When complex neuronal structures may not matter

  1. Adriane G Otopalik  Is a corresponding author
  2. Alexander C Sutton
  3. Matthew Banghart
  4. Eve Marder  Is a corresponding author
  1. Brandeis University, United States
  2. Harvard Medical School, United States
11 figures, 2 tables and 2 additional files

Figures

The stomatogastric nervous system (STNS) and identification of gastric mill (GM) neurons.

(A) Schematic of an in vitro, isolated STNS with descending inputs intact (from bilateral commissural ganglia (CoGs) and esophogeal ganglion (OG)). The stomatogastric ganglion (STG; green box) …

https://doi.org/10.7554/eLife.23508.002
GM neurons exhibit expansive and complex morphologies.

(A) Maximum z-projections of 3-dimensional confocal image stacks capturing Lucifer yellow dye-fills of six GM neurons (taken at 20x magnification). (B) Skeletal reconstructions of the six neurons …

https://doi.org/10.7554/eLife.23508.003
Variable axon location and branching patterns in GM neurons.

(A) Histogram shows the number of distinguishable axonal projections for 14 GM neurons. (B) Histograms show the distribution of branch orders across 14 GM neurons. Axonal branch point orders are …

https://doi.org/10.7554/eLife.23508.004
Figure 4 with 1 supplement
Focal glutamate responses across GM neuronal structures.

(AC) show maximum z-projections of confocal stacks of neuronal dye-fills with photo-uncaging sites indicated with colored circles. In each case, raw traces are shown on the right for maximal …

https://doi.org/10.7554/eLife.23508.005
Figure 4—figure supplement 1
Focal glutamate photo-uncaging resolution and response desensitization.

(A) Image of UV spot emission in fluorescein solution (top). Line intensity. profile (bottom) shows a saturated spot diameter of ~15 microns. (B) (i) Maximum projection of a confocal image stack of …

https://doi.org/10.7554/eLife.23508.006
Figure 5 with 1 supplement
Response amplitudes as a function of various cable properties.

Each lolliplot shows the normalized maximal response amplitudes for photo-uncaging sites that vary in distance from the soma, branch order, and neurite diameter. Each color is indicative of focal …

https://doi.org/10.7554/eLife.23508.007
Figure 5—figure supplement 1
Response amplitudes as a function of various cable properties with raw response amplitudes and linear fits.

Each lolliplot shows the maximal response amplitudes in mV for photo-uncaging sites that vary in distance from the soma, branch order, and neurite diameter. Each color is indicative of focal …

https://doi.org/10.7554/eLife.23508.008
Figure 6 with 1 supplement
Passive cable simulations show that apparent Erev measurements are independent of maximal conductance (gmax) and dependent on the distance between activation and recording sites.

(A) An inhibitory current (actual Erev = −70 mV, τ = 3 ms) was activated 200 µm from the recording site (at 0 µm). (B) Voltage events as measured at 0 µm. The membrane potential at the recording …

https://doi.org/10.7554/eLife.23508.010
Figure 6—figure supplement 1
The apparent Erev remains independent of gmax, regardless of the activation site’s distance from the recording site.

An inhibitory current (actual Erev = −70 mV) was evoked at varying distances from the recording site 0 µm. (AF) All plots show apparent Erevs as a function of gmax (1, 5, 10, 50 nS) for all 20 …

https://doi.org/10.7554/eLife.23508.011
The shift in apparent Erev with activation site distance is contingent upon the electrotonic length constant, λ.

(A) For each of the 20 cable models, with varying passive properties and, consequently, λ values (see Materials and methods), an inhibitory current (actual Erev = −70 mV) was evoked at varying …

https://doi.org/10.7554/eLife.23508.012
Figure 8 with 1 supplement
Reversal potentials are nearly invariant across individual neuronal structure.

(A) Photo-uncaging sites are indicated as unique colors on the skeletal reconstruction of one GM neuron. (B) Raw voltage traces show focal glutamate responses as measured at the soma in …

https://doi.org/10.7554/eLife.23508.013
Figure 8—figure supplement 1
Reversal Potentials are nearly invariant across individual neuronal structure, a second example.

(A.) Photo-uncaging sites are indicated as unique colors on the skeletal reconstruction of one GM neuron. (B) Raw voltage traces show focal glutamate responses as measured at the soma in …

https://doi.org/10.7554/eLife.23508.014
Figure 9 with 1 supplement
Reversal potentials as a function of various cable properties.

Each lolliplot shows the glutamate response apparent reversal potentials (Erevs) for photo-uncaging sites as function of their distance from the soma, branch order, and neurite diameter. Each color …

https://doi.org/10.7554/eLife.23508.016
Figure 9—figure supplement 1
Reversal potentials as a function of various cable properties with linear fits.

Each lolliplot shows the glutamate response apparent reversal potentials (Erevs) for photo-uncaging sites as function of their distance from the soma, branch order, and neurite diameter. Each color …

https://doi.org/10.7554/eLife.23508.017
Microscope schematic showing laser (purple), fluorescence excitation (blue), and fluorescence emission (green) paths.

A 1 Watt 355 nm laser (1) is focused by a plano-convex lens (2) and coupled to a 50-micron fiber optic cable (3) situated on an x-y translating fiber adaptor (4). The UV beam is collimated with a …

https://doi.org/10.7554/eLife.23508.018
Passive parameters used for cable model library.

All pairwise combinations. of passive conductance (gpas; 5, 10, 20, 50 nS/cm2) and axial resistance (Ra; 1, 5, 10,. 30, 50 Ω•cm) values were used to generate a library of 20 cable models with …

https://doi.org/10.7554/eLife.23508.019

Tables

Table 1

Linear regression analysis for response amplitudes as a function of distance, branch order, and neurite diameter. Each row corresponds to a different GM neuron, with same color scheme, as shown in Fi…

https://doi.org/10.7554/eLife.23508.009

Distance

Branch order

Diameter

Neuron

MSE

R

p

slope (mV/um)

MSE

R

p

slope (mV/order)

MSE

R

p

slope (mV/um)

n

0.11

−0.27

0.418

−0.0009

0.12

−0.20

0.55

−0.0104

0.10

0.39

0.24

0.1028

11

0.02

0.28

0.592

0.0003

0.02

0.26

0.62

0.0052

0.03

0.01

0.99

0.0007

7

0.03

−0.19

0.656

−0.0003

0.03

−0.21

0.62

−0.0057

0.02

−0.44

0.28

−0.0331

9

0.59

0.42

0.229

0.0026

0.51

0.54

0.11

0.0472

0.57

−0.45

0.19

−0.1713

11

0.14

0.22

0.679

0.0005

0.14

0.23

0.66

0.0100

0.12

−0.48

0.33

−0.0680

7

0.01

0.90

0.002

0.0013

0.02

0.68

0.07

0.0232

0.01

−0.75

0.03

−0.0728

9

0.02

-−0.49

0.269

−0.0005

0.03

−0.44

0.33

−0.0073

0.03

0.32

0.48

0.0338

8

0.11

0.20

0.443

0.0008

0.11

0.24

0.35

0.0142

0.10

−0.37

0.14

−0.0682

18

0.02

0.26

0.579

0.0004

0.02

0.32

0.49

0.0060

0.01

−0.60

0.16

−0.0244

8

0.32

−0.27

0.477

−0.0021

0.25

−0.53

0.15

−0.0455

0.25

0.51

0.16

0.3891

11

Mean

0.14

0.11

0.434

0.0002

0.12

0.09

0.39

0.0037

0.12

−0.19

0.30

0.0089


SD

0.18

0.41

0.214

0.0013

0.15

0.41

0.23

0.0242

0.17

0.45

0.27

0.1520


Table 2

Linear regression analysis for reversal potentials as a function of distance, branch order, and neurite diameter. Each row corresponds to a different GM neuron, with same color scheme, as shown in Fi…

https://doi.org/10.7554/eLife.23508.015

Reversal potentials

Distance

Branch order

Diameter

Neuron

Mean (mV)

SD

CV

MSE

R

p

slope (mV/um)

MSE

R

p

slope (mV/order)

MSE

R

p

slope (mV/um)

n

Rinput (MΩ)

−73.8

2.9

−0.04

5.99

0.44

0.18

0.012

6.52

0.35

0.30

0.139

6.52

0.34

0.30

0.712

11

10

−79.2

1.2

−0.02

1.21

0.00

0.99

0.000

1.16

−0.21

0.68

−0.029

0.54

−0.75

0.09

−0.513

6

15

−81.9

3.2

−0.04

8.80

0.14

0.76

0.006

8.86

0.12

0.80

0.071

5.86

−0.59

0.16

−1.123

7

12

−83.6

4.3

−0.05

13.13

0.45

0.23

0.013

13.35

0.43

0.24

0.175

14.39

−0.35

0.35

−0.613

9

12

−75.6

3.8

−0.05

9.42

0.15

0.90

0.0010

9.61

-0.05

0.97

−0.058

0.34

−0.98

0.12

−10.756

3

11

−87.7

2.7

−0.03

5.18

0.34

0.51

0.009

5.27

0.32

0.54

0.142

5.20

0.34

0.51

0.478

6

7

−64.8

3.6

−0.06

8.59

−0.50

0.26

−0.011

7.53

−0.58

0.17

−0.185

11.38

−0.04

0.93

−0.084

7

5

−69.9

3.3

−0.05

9.37

−0.22

0.46

−0.008

9.01

−0.29

0.33

−0.146

9.84

0.05

0.87

0.015

11

7

−84.6

3.0

−0.04

7.88

-−0.02

0.97

−0.001

7.80

0.10

00.83

0.039

7.88

−0.0

0.96

−0.020

7

10

−85.0

2.2

−0.03

3.02

−0.53

0.28

−0.042

4.11

0.13

0.80

0.144

2.84

0.57

0.24

1.805

6

10

Pooled Mean

−78.6

−0.04

7.26

0.03

0.55

−0.001

7.32

0.03

0.57

0.029

6.48

−0.14

0.45

−1.010


9.9

Pooled SD

7.4



3.47

0.35

0.32

0.016

3.34

0.32

0.29

0.128

4.57

0.51

0.34

3.518


2.9

Additional files

Supplementary file 1

Neuronal Structure Hoc files.

https://doi.org/10.7554/eLife.23508.020
Supplementary file 2

Uncaging Coordinates Hoc files.

https://doi.org/10.7554/eLife.23508.021

Download links