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First published online March 9, 2004
Journal of Experimental Biology 207, 1361-1368 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00885

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Contribution of eye retraction to swallowing performance in the northern leopard frog, Rana pipiens

Robert P. Levine^1,*, Jenna A. Monroy² and Elizabeth L. Brainerd¹

¹ Biology Department and Organismic and Evolutionary Biology Program, University of Massachusetts Amherst, 611 North Pleasant St, Amherst, MA 01003, USA
² Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, USA

View larger version (60K): [in a new window]   Fig. 1. Video frames from a swallowing sequence illustrating (A) the normal position of the eyes; (B) head extension and lordosis of the vertebral column during initial eye retraction; (C) full eye retraction and (D) a kinematic trace of the percent eye retraction versus time for the same swallowing sequence. The arrows in D, labeled A, B and C, correspond with the frames from the swallowing sequence. Note that eye retraction is rapid, the eyes remain retracted for a relatively long time, more than 0.5 s in this example, and then eye protraction is slower than eye retraction. A representative video of Rana pipiens swallowing a cricket can be viewed online (http://jeb.biologists.org/).

View larger version (82K): [in a new window]   Fig. 2. Selected x-ray video frames of Rana pipiens swallowing a cricket, illustrating the movement of the eyes during feeding. Lead balls (arrow A) mark the insertion of the retractor bulbi on the ventral surface of the eyes. A cricket has been marked with barium powder (arrow B) to facilitate viewing in x-ray. Note that as the eyes retract into the oropharynx, the cricket moves back towards the esophagus. Time (seconds) is indicated on each frame. A representative x-ray video of Rana pipiens swallowing a cricket can be viewed online (http://jeb.biologists.org/).

View larger version (21K): [in a new window]   Fig. 3. Electromyographic (EMG) activity from the right (RRB) and left (LRB) retractor bulbi muscles of Rana pipiens during swallowing. Black bars represent the duration of each eye retraction and were calculated from synchronized light video. Line drawings represent the position of the eyes during periods of relaxation (A,C) and during active retraction of the eyes (B,D). Note that bilateral EMG activity starts shortly before eye retraction begins and ends as the eyes return to their rest positions.

View larger version (22K): [in a new window]   Fig. 4. Bar chart of the mean number of swallows for each individual frog for the three treatment groups: control, sham and denervation. Each bar represents the mean (± S.E.M.) of five feeding trials for one individual (N=8 individuals per treatment, five feedings per individual). One-way ANOVA with Tukey post-hoc tests revealed a significant difference between the control and the denervation groups and the sham and the denervation groups but no difference between the control and sham group (see Table 1).