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A pair of motion-sensitive neurons in the locust encode approaches of a looming object

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Abstract

Neurons in the locust visual system encode approaches of looming stimuli and are implicated in production of escape behaviours. The lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD) compute characteristics of expanding edges across the locust eye during a loom and DCMD synapses onto motor elements associated with behaviour. We identified another descending interneuron within the locust ventral nerve cord. We named this neuron the late DCMD (LDCMD) as it responds later during an approach, with the firing rate peaking at about the time of collision. LDCMD produced lower amplitude, broader action potentials that were associated with an afterhyperpolarization, whereas DCMD action potentials showed a brief afterhyperpolarization often followed by an afterdepolarization. Within the mesothoracic ganglion, the primary LDCMD axon located adjacent to the DCMD axon, was thinner and lacked collateral projections to the lateral region of the neuropil. When compared with DCMD, LDCMD fired with fewer spikes during a loom and showed weaker habituation to repeated approaches. Coincidence of LDCMD and DCMD firing increased during object approach. Our findings indicate the presence of an additional motion-sensitive descending neuron in the locust that encodes temporally distinct properties of an approaching object.

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Acknowledgments

We thank T. G. A. Money for providing valuable comments on an earlier version of the manuscript. This work was supported by grants from the Natural Science and Engineering Research Council of Canada (NSERC) to J. R. Gray and R. M. Robertson as well as a University of Saskatchewan Graduate Teaching Fellowship to E. Blincow.

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Authors and Affiliations

  1. Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada

    John R. Gray & Eric Blincow

  2. Department of Biology, Queen’s University, Kingston, ON, K7L 3N6, Canada

    R. Meldrum Robertson

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  1. John R. Gray
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  2. Eric Blincow
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  3. R. Meldrum Robertson
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Correspondence to John R. Gray.

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359_2010_576_MOESM1_ESM.pdf

Quantification of neuronal firing parameters. A sample peristimulus time histogram of the DCMD response to a looming disc aligned to time of projected collision (TTC = 0 s). The firing parameters measured were the maximum firing rate (dashed line), the time of peak firing (*), the width of the response profile at ½ maximal firing (dotted line), the firing rate 200 ms before collision and the number of spikes

359_2010_576_MOESM2_ESM.pdf

Habituation of LDCMD and DCMD response profiles from a single representative locust. Each plot is a Gaussian smoothed (50 ms bin width) peristimulus time histogram of a response to a single approach within a consecutive series of twenty approaches (from top to bottom, respectively). In this example the DCMD habituated quickly and stopped responding after the tenth approach whereas the LDCMD habituated within the first three approaches but continued to respond throughout the series. Data were aligned to TOC (red vertical line)

359_2010_576_MOESM3_ESM.pdf

Relative habituation of LDCMD and DCMD firing parameters. Data from the final approach in a series of 8 to 50 approaches were normalized to the value in response to the first approach. Larger values indicate weaker habituation. LDCMD habituated less with respect to all parameters measured. Parametric data in a and b (bar charts) were compared with a student’s t-test whereas non parametric data in c and d (box plots) were compared with a Mann–Whitney rank sum test. Error bars in a and b represent standard deviation. Boxes in c and d indicate interquartile range and median value, whiskers indicate the 5 and 95% confidence levels and dots indicate range. Different letters above each bar or box indicate significant differences. n = 8 locusts

359_2010_576_MOESM4_ESM.pdf

Power spectral densities of LDCMD (red) and DCMD (black) firing during presentation of looming stimuli. A prominent peak at 65 Hz in the DCMD spectrum (arrow) is absent from the LDCMD spectrum. Spectra were normalized such that the sum of all spectra for each neuron was set to 100. Data were selected from 70 single approaches to 29 locusts

359_2010_576_MOESM5_ESM.pdf

Assessment of the significance of the JSPTH matrix bin counts. The bin counts are represented as the logarithm of the derived probability of a binary representation within each bin. Coincidence was assumed to be binary (1 or 0) where bins based on random firing would not have a value greater than 1. The actual bin counts, represented by the colour scale, clearly show many values > 1, strongly indicating that coincidence firing in those bins was not due to chance

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Gray, J.R., Blincow, E. & Robertson, R.M. A pair of motion-sensitive neurons in the locust encode approaches of a looming object. J Comp Physiol A 196, 927–938 (2010). https://doi.org/10.1007/s00359-010-0576-7

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