Optimal searching behaviour generated intrinsically by the central pattern generator for locomotion

  1. David W Sims  Is a corresponding author
  2. Nicolas E Humphries
  3. Nan Hu
  4. Violeta Medan
  5. Jimena Berni  Is a corresponding author
  1. The Marine Biological Association of the United Kingdom, United Kingdom
  2. University of Southampton, United Kingdom
  3. University of Cambridge, United Kingdom
  4. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Argentina
  5. Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-UBA-CONICET), Argentina
8 figures, 5 tables and 8 additional files

Figures

Testing for Lévy-like search patterns in Drosophila larva tracks.

(A) Computer simulated path with Lévy-distributed move step lengths (truncated power-law exponent, µ = 2.0) between turning points. (B) Rank step-length-frequency distribution of steps in (A) with …

Figure 2 with 3 supplements
Estimating move step lengths in Drosophila larva tracks across broad scales.

(A) Examples of track processing and turn identification. Row 1, column one shows an example of the effect of the Kalman filter on raw track data; column two shows the steps and turns that would …

Figure 2—figure supplement 1
Analysis of curved paths.

Drosophila larva sometimes exhibit curved paths within movement trajectories. (A) This shows an example of a Kalman filtered track of a control larva (BL/+ at 33°C) executing a curved path. The …

Figure 2—figure supplement 2
Effects of Kalman filter parameter changes on an example larva track.

(A) The first 10 min of a raw, unprocessed larva track compared with (B) the same track subjected to the Kalman filter (KF) parameters used for the main analysis presented in the main paper. Note …

Figure 2—figure supplement 3
Effect of edge collision on search strategy.

Comparison of μ exponents of the truncated Lévy power-law best model fits to exploration patterns of control animals (BL/ + and shits/+ control larvae at 22°C and 33°C) before and after a collision …

Effect of temperature on activity and feeding.

(A) The curve of inactivation of synaptic transmission with increasing temperature demonstrated by decrease in the average velocity of elav-Gal4/UAS shits third instar larvae as a function of …

Shibirets mediated inhibition of brain activity.

(A–B) Schematic of the experimental design for extracellular recordings. (A) Early third instar larvae were dissected and a suction electrode was attached to one brain lobe. NC denotes the nerve …

Figure 5 with 1 supplement
Control and brain blocked larvae movements.

Example of larva trajectories for each of 8 experimental treatments. Each treatment is signified by the Drosophila brain outlines and colour coding on the left of panels (A). BL/+ (light grey) and sh…

Figure 5—figure supplement 1
The distributions of turning angles along larva paths.

Comparison of (A) the raw distribution of turn angles with (B) the turn angle distribution after determining significant turns. The raw distribution in (A) is dominated by a very high frequency of …

Summary data of truncated power law exponents across treatments.

(A) Images and diagrams of the pattern of expression targeted in each genotype. (B) Comparison of μ exponents of the truncated Lévy power-law best model fits to exploration patterns of BL/ + and shit…

Near optimal Lévy search in larvae after apoptosis in the brain lobes.

(A) Expression pattern of the BLsensR57C10 line. Gal4 is highly expressed in the brain lobes and SOG until the anterior boundary of SCR expression. (B) Schematic of the experimental design. Each one …

Example tracks in larva after apoptosis in the brain lobes.

(A) Control BLsens > rpr,hid larvae at 22°C show movement patterns, path complexity and truncated power law best fits that are similar to (B) BLsens > rpr,hid larvae at 32°C with apoptosis in the …

Tables

Table 1
Tortuosity (cluster) analysis MLE results.

Summary of mean μ exponents and orders of magnitude of the data range fitted by truncated power-law model fits from tortuosity analysis. T (°C) denotes different environmental temperature of …

T (°C)TreatmentNo. ofTracksMean µSDOrders of
Magnitude
SD
22BL/+291.700.341.980.41
33BL/+311.540.381.990.62
22shits /+331.850.441.890.39
33shits /+341.610.402.040.40
33MB247/+ 211.390.271.870.45
33BLsens > shits61.750.651.370.51
33BL > shits231.670.401.610.61
33MB247 > shits221.350.181.930.34
22New Blsens > rpr,hid_control611.740.332.110.37
32New BLsens > rpr, hid221.410.291.550.26
Table 2
MLE Analysis summary.

Summary of mean μ exponents and orders of magnitude of the data range fitted by truncated power-law model fits across experimental treatments. T (°C) denotes different environmental temperature of …

T (°C)TreatmentN tracksMuSDOrders of magnitude of the dataSD
22BL/+301.470.361.630.42
33BL/+331.350.321.480.49
22shits/+341.490.351.520.32
33shits /+391.540.431.520.38
33MB247/+231.740.481.330.44
33BL > shits261.660.501.150.40
33BLsens > shits111.960.391.200.23
33MB247 > shits231.560.351.390.46
22BLsens > rpr, hid_control621.510.381.710.40
32BLsens > rpr, hid232.140.470.930.52
Table 3
Cumulative probability distributions.

Cumulative probability distributions of truncated power law exponents calculated from individual larva move-step length distributions across experimental treatments. T (°C) denotes different …

Cumulative Probability Distribution (%)
T (°C)Treatmentμ exponent range
1–31.25–2.751.5–2.51.75–2.25
22BL/+93.271.241.317.1
33BL/+90.459.626.48.1
22shits /+98.476.833.68.0
33MB247/+96.283.960.230.6
33BL > shits92.576.051.625.3
33BLsens > shits98.795.180.647.3
33MB247 > shits96.679.950.622.4
22BLsens > rpr, hid_control94.875.045.219.3
32BLsens > rpr, hid92.985.167.938.4
Table 4
MSD analysis results.

Mean and standard deviations for the values of alpha and R2 from the mean squared displacement analysis. T (°C) denotes different environmental temperature of treatment.

T (oC)TreatmentNo. of
tracks
Mean αSDMean R2SD
22BL/+301.340.510.880.10
33BL/+331.410.530.900.10
22shits /+341.260.450.880.16
33shits /+391.370.730.830.21
33MB247/+231.400.810.840.12
33BL> shits261.210.550.810.24
33BLsens> shits110.940.780.670.25
33MB247> shits231.030.420.800.18
22New BLsens> rpr,hid_control621.170.490.810.20
32New BLsens> rpr, hid231.300.530.800.14
Key resources table
Reagent type
(species) or resource
DesignationSource or
reference
IdentifiersAdditional
information
Strain, strain background
(Drosophila
melanogaster)
w; elav-GAL4,
tsh-GAL80/ +,+; cha3.3-GAL80,
UAS-EGFP/ +
DOI:
10.1016/j.cub.2012.07.048
NABL/+
Strain, strain
background (Drosophila melanogaster)
w; elav-GAL4, tsh-GAL80/ +,+; cha3.3-GAL80, UAS-EGFP / +DOI:10.1016/j.cub.2012.07.048NABL > +
Strain, strain
background
(Drosophila melanogaster)
w; elav-GAL4, tsh-GAL80/ +,+; UAS-EGFP / +DOI:
10.1016/j.cub.2012.07.048
NABLsens > +
Strain, strain background (Drosophila
melanogaster)
20XUAS-IVS-Syn21-Shibire-ts1-GFP-p10Gift from G. RubinNA
Strain, strain background (Drosophila melanogaster)MB247-GAL4Gift form J. NgNA
Strain, strain background (Drosophila
melanogaster)
UAS-rpr, UAS-hidGift from from M. LandgrafNA
Strain, strain
background (Drosophila melanogaster)
UAS-myrRFPGift from from
M. Landgraf
NA
Strain, strain
background (Drosophila melanogaster)
P{GMR57C10-GAL4}attP2Bloomington
Drosophila Stock Center
RRID:BDSC_39171In attp40
Strain, strain background
(Drosophila
melanogaster)
P{tubP-GAL80[ts]}2Bloomington Drosophila Stock CenterRRID:BDSC_7017
ChemicalPoly-L-Lysine
hydrobromide
SigmaP2524
AntibodyMouse monoclonal
anti-SCR
Development Studies
Hybridoma Bank (DSHB), IA, USA
RRID:AB_5284621:
20 dilution
AntibodyChicken polyclonal anti-GFPabcamab139701/2000 dilution
AntibodyRabbit polyclonal anti-Cleaved
Drosophila
Dcp-1(Asp216)
Cell Signaling Technology#95781/100
AntibodyDonkey polyclonal
Alexa568 anti-mouse
InvitrogenA10042
1/500
AntibodyDonkey polyclonal CF633 anti-rabbitBiotumBT201251/500 dilution
AntibodyGoat polyclonal Alexa488 anti-chickenBiotumBT200201/500
Software
FIMTrackhttps://www.uni-muenster.de/PRIA/en/FIM/download.shtmlNAFIMTrack_v2_X64_MacOS
SoftwareMBA MLE Analysishttp://dx.doi.org/10.1111/2041-210X.12096NA
Softwareclampfithttps://moleculardevices.app.box.com/s/l8h8odzbdikalbje1iwj85x88004f588NA

Additional files

Supplementary file 1

Summary of larvae tracked and the model fits.

The number of trials and number of larvae tracked per trial is given along with the move-step frequency distribution model fitting and model selection results for all trials across experimental treatments. The number of larvae paths in TP denotes the number of individual path best fits to a truncated Pareto (power law) distribution; E, the number best fitting an exponential distribution; and U is unclassified where there was no clear best fit to either model. Tracks discarded prior to model fitting were those where larvae collided, the arena edge was encountered, or there were <50 fitted movement steps. Maximum Likelihood Estimation (MLE) was used for parameter fitting (exponent, xmax) and Akaike’s Information Criteria weights (wAIC) used for model selection. For full description of procedures used see Methods.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp1-v3.xlsx
Supplementary file 2

Sensitivity analyses for Kalman filter parameters and minimum step resolution values.

(A) Kalman filter (KF) parameters and (B) minimum step resolution values were altered to determine the effects of such changes on the consistency of treatment µ values. The values used for the results presented in the main paper were Position and Velocity minimum variances of 0.5 and a covariance of 1.0 for the KF, and a minimum step resolution of 0.44. The sensitivity analysis for the KF parameters considered values that differed significantly from those used, bracketing the analysis values. As can be seen in (A), differences in the µ values were generally small, confirming that the values chosen for the KF did not alter the finding of truncated power-laws in larva tracks. Rather, the average µ values from all KF sensitivity tests are close to those found in the analysis. The minimum step resolution value chosen for the analysis (0.44) was determined from the tracking resolution and larval movements (head sways and peristaltic contractions) and represents the lowest value above the track noise. All computed move steps lower than this value were excluded from the analysis. For the sensitivity test, values of 0.3, 0.5, 0.7 and 0.9 were used as this range covered viable alternative values. As with the KF tests, the finding of truncated power-laws and the resultant µ values differed very little from those presented in the original analysis. We conclude that significant changes in parameters associated with video track processing had no important effects on our finding of truncated power-laws in larva movement paths and the resultant µ values.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp2-v3.docx
Supplementary file 3

Summary of results for truncated Pareto model fits compared to exponential model distributions.

Full MLE results of truncated power law fits to larvae move step-length frequency distributions across trials and experimental treatments.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp3-v3.xlsx
Supplementary file 4

Summary of results for truncated Pareto model fits compared to other model distributions.

Model selection using Akaike’s Information Criteria weights (wAIC) from comparison of the log likelihoods (LLH). For full description of procedures see Materials and methods. TP, truncated Pareto distribution fit to larva move-step frequency distribution; P, power law; E, exponential; TE, truncated exponential; LN, log-normal; G, gamma distribution. Values in model columns denote best fit based on wAIC. Note the high number of larva best fit by TP model distributions when compared with other models.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp4-v3.xlsx
Supplementary file 5

Tests for stationarity in the larva movement pattern data within treatments.

Larva tracks with fitted move steps were separated at the midpoint and those for which each half was best fitted by a truncated power-law were retained for analysis. The average µ values for the first and second half of all tracks across trials within a treatment were compared to determine any significant differences, which would indicate changes in track statistics over time (i.e. non-stationarity). We found no significant differences between the first and second halves of the tracks and with no clear trend of increasing or decreasing µ values, as might be expected to occur if µ showed significant temporal dependence on changing satiety or other factors over the 1 hr trial period.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp5-v3.docx
Supplementary file 6

Summary of model comparisons.

Model comparisons for each larva path across trials and experimental treatments is given (wAIC) for the truncated Pareto (TP), exponential (Exp), power-law (P) and composite Brownian (CB) model distributions with proportions of two (CB2), three (CB3) and four exponentials (CB4). Bold wAIC values denote best fit. Note the high number of larva best fit by TP model distributions when compared with other models.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp6-v3.xlsx
Supplementary file 7

Video frame frequency test.

Ten shits/+ larvae at 33°C were tracked with a video frame capture rate set at 15 frames per second (fps; Hz). These data were then subsampled to 7.5, 5 and 3 Hz to test whether video frame frequency affected estimation of the μ exponent following MLE analysis and model selection. A Kruskal-Wallis test showed no differences between medians of truncated power law μ exponents across the four different frequencies (H(3)=3.9, p=0.271) indicating video frame rate did not contribute significantly to determination of μ exponent values.

https://cdn.elifesciences.org/articles/50316/elife-50316-supp7-v3.xlsx
Transparent reporting form
https://cdn.elifesciences.org/articles/50316/elife-50316-transrepform-v3.docx

Download links