Behavioral Lateralization and Optimal Route Choice in Flying Budgerigars

<div><p>Birds flying through a cluttered environment require the ability to choose routes that will take them through the environment safely and quickly. We have investigated some of the strategies by which they achieve this. We trained budgerigars to fly through a tunnel in which they encountered a barrier that offered two passages, positioned side by side, at the halfway point. When one of the passages was substantially wider than the other, the birds tended to fly through the wider passage to continue their transit to the end of the tunnel, regardless of whether this passage was on the right or the left. Evidently, the birds were selecting the safest and quickest route. However, when the two passages were of equal or nearly equal width, some individuals consistently preferred the left-hand passage, while others consistently preferred the passage on the right. Thus, the birds displayed idiosyncratic biases when choosing between alternative routes. Surprisingly - and unlike most of the instances in which behavioral lateralization has previously been discovered - the bias was found to vary from individual to individual, in its direction as well as its magnitude. This is very different from handedness in humans, where the majority of humans are right-handed, giving rise to a so-called ‘population’ bias. Our experimental results and mathematical model of this behavior suggest that individually varying lateralization, working in concert with a tendency to choose the wider aperture, can expedite the passage of a flock of birds through a cluttered environment.</p></div

A. Illustration of total transit times as predicted by a model of a flock of budgerigars negotiating two simultaneously presented apertures of width d mm (left-hand aperture) and (D-d) mm (right-hand aperture), where D, the sum of the widths of the two apertures, is 100 mm.

<p>The curves show the variation of the total transit time with d for strategies A (blue), B (green), C (black), D (dashed black) and E (red), as described in the text. For clarity, the curve for strategy D is shown displaced slightly upwards. <b>B</b>. Probability functions for the choice of the left-hand aperture (blue curve) and the right-hand aperture (red curve) as a function of the width d of the left-hand aperture, for the optimum strategy (E) described in the text. <b>C</b>. Model showing choice probability for the left-hand aperture as a function of its width, for individual birds with a range of different bias parameters (B) varying from 0 mm to 100 mm in steps of 10 mm. The choice probability for each bird is modeled by a step function (dashed blue curve). The continuous red curve shows the resulting average choice probability function for the entire flock. <b>D</b>. Choice probability functions for the left-hand aperture for individual birds with a range of different bias parameters (B) varying from 0 mm to 100 mm in steps of 10 mm. The choice probability for each bird is modeled by a logistic function (dashed blue curve). The continuous red curve shows the resulting average choice probability function for the entire flock.</p

Results of fit of data to a logistic function (equation (24)) with parameters B, α, and <i>Δd</i>, as described in the text and “Methods.”

<p>The numbers show estimated values and 95% confidence limits. The asterisks identify values of B that are significantly different from 50.0, indicating a significant bias.</p

Experimental configuration.

<p>Details in text.</p

Widths of left-hand and right-hand apertures.

<p>Widths of left-hand and right-hand apertures.</p

Logistic function used to quantify aperture discrimination.

<p>Details in text.</p

Illustration of a hypothetical example in which there are four apertures: A, B, C and D.

<p>Details in text.</p

(A–E) Aperture choice profiles for birds <i>One, Casper, Two, Drongo</i> and <i>Saras</i>, showing choice frequencies for the left-hand aperture as a function of its width.

<p>The dashed vertical line represents the condition when both apertures are of equal width (50 mm). The dashed horizontal line represents the random-choice level of 50%. The symbols next to each data point indicate a statistically significant difference of the choice frequency from the random-choice level of 50%, calculated as described in ‘<a href="http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003473#s4" target="_blank">Methods</a>’. [p<0.05: (*); p<0.02: (**) and p<0.00001: (***)]. The red dashed curve in each panel displays a fit of the data to a logistic function, as described in the Supporting Information. (<b>F</b>) Average preference for the left-hand aperture as a function of its width, obtained by pooling the aperture choice profiles of all 5 birds (Fig. 3A–E). The fitted values of the parameters B and Δd of the logistic function are shown in each panel. The horizontal red error bar in each panel represents the 95% confidence interval for the estimated value of B.</p

Examples of birds choosing between two apertures.

<p>The red arrow denotes the direction of bird flight. The widths of the left- and right-hand apertures are respectively 60 mm and 40 mm in (A), 90 mm and 10 mm in (B), and 0 mm and 100 mm in (C).</p

The activity of model V1 complex neurons.

<p>Each graph shows the activity of the V1 complex neurons selective to the direction shown by the colored arrow. The angle of each arrow also indicates its direction. The axes represent the location and the gray scale intensity indicates the level of activity. Neurons at the edges have higher activity compared to neurons at the terminators, which have unambiguous motion signals. The cartoon in the middle summarizes the results shown in eight graphs. The colored section of the bar shows neurons selective to the directions that have the highest levels of activity at those locations. For a bar moving towards the right, the terminators, indicated by the purple color, show the correct direction of motion; the colors of the edges represent the directions that are incorrect because of the aperture problem.</p