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Kinematics of the buccal mass during swallowing based on magnetic resonance imaging in intact, behaving Aplysia californica

David M. Neustadter^1,2, Richard F. Drushel³ and Hillel J. Chiel^1,3,4,*

¹ Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH 44106-7080, USA
² MR Systems Department, G. E. Medical Systems Israel Ltd, Keren Hayesod Street, PO Box 2071, Tirat Carmel 39120, Israel
³ Department of Biology, Case Western Reserve University, Cleveland, OH 44106-7080, USA
⁴ Department of Neurosciences, Case Western Reserve University, Cleveland, OH 44106-7080, USA

View larger version (27K): [in a new window]   Fig. 1. Key components of the magnetic resonance imaging techniques for intact, behaving Aplysia californica. (A) Imaging sequence. Gradient echo planar imaging (EPI) sequence with TR (acquisition time)=155 ms, TE (time to echo)=73 ms, acquisition matrix=64x128; FOV (field of view)=6.4 cmx12.8 cm; slice thickness=3 mm. RF, radio frequency. (B) The imaging tank and coil showing the opening through which Aplysia californica is inserted after being placed in the slug holding capsule. (C) The slug holding capsule showing the food spool, seaweed extract tube and strings for positioning the capsule within the tank.

View larger version (106K): [in a new window]   Fig. 2. Determining that the mid-sagittal image is correctly oriented. The mid-sagittal image is shown at the bottom. The right of the figure is anterior (the jaws of the animal) and left of the figure is posterior (the lumen of the gut and the esophagus are visible and labelled; this convention for positioning mid-sagittal images will be used throughout the paper). The coronal image that was recorded 155 ms before this mid-sagittal image is shown in the middle (right is anterior, left is posterior) and the axial image recorded 155 ms after this mid-sagittal image is shown at the top (left is dorsal, right is ventral). Note that the orthogonal images are both symmetrical and centered around the midline, providing evidence that the sagittal image is neither para-sagittal nor significantly rotated.

View larger version (56K): [in a new window]   Fig. 3. Mid-sagittal anatomy of buccal mass and radular stalk measurements. Key anatomical features visible in mid-sagittal fixed tissue (A) and in high-spatial-resolution magnetic resonance (MR) images (B) are indicated. The features outlined in the high-temporal-resolution MR images (see Fig. 4) are visible. To create a reference length for measurements that could be reliably measured on the high-temporal-resolution MR images, the length of the inner width of the radular stalk was used. To relate this width to external measurements of radular stalk width, we measured the ratio of the outer to the inner widths in fixed tissue (A), in high-resolution MR images (B) and in freshly dissected tissue (not shown). (C) Radular stalk shape based on a three-dimensional reconstruction of high-resolution MR images. (D) Mid-sagittal view of radular stalk shape based on the three-dimensional reconstruction shown in C.

View larger version (110K): [in a new window]   Fig. 4. Measurements on high-temporal-resolution magnetic resonance images. The same image is shown in A-D. (A) Radular stalk outline (see Fig. 3 and text) and a line indicating the axis of the radular stalk. (B) The angle of the anterior margin of the odontophore, determined by the margin of the I6 muscle just posterior to the prow (see Fig. 6 and text). (C) Outline of the odontophore including the prow. (D) Image showing all the measurements shown in A-C and, in addition, an outline of the entire buccal mass (excluding the pharyngeal tissue), the line of the jaws and the line of the lateral groove (the dorsal and ventral border between the I1/I3/jaw musculature and the posterior I2 muscle).

View larger version (133K): [in a new window]   Fig. 5. A sequence (frames 1-22) showing swallowing of a polyethylene tube and its associated kinematic measures. Frames are acquired in 155 ms and are separated by 310 ms. The top row shows the high-temporal-resolution data; the middle row shows these images with the kinematic measures (described in Fig. 4) superimposed and the bottom row shows the kinematic measures alone. This corresponds to swallow 4, data for which are shown in part D of Figs 7,8,9,10,11,12,13.

View larger version (64K): [in a new window]   Fig. 6. Anatomy of the prow of the odontophore. (A) External anatomy, anterior view. (B) External anatomy, lateral view. (C) External anatomy, dorsal view. The prow shown in these views was approximately 4 mm in medio-lateral length, 8 mm in dorso-ventral length and 4 mm in antero-posterior length. (D) Internal muscle fibers of the prow. The view is posterior, looking at the inside of the antero-medial surface of the prow.

View larger version (19K): [in a new window]   Fig. 7. Kinematics of the I2 muscle during swallowing. Data in A-D are plotted as length (mm) as a function of time (ms). (A) I2 kinematics in the first swallow. The first sequence from the images in set 7725 starts with image 27 and ends with image 44. The onset of the t4 period is frame 27, the onset of the t1 period is frame 32 and the onset of the t2 period is frame 41; each of these period onsets is indicated using a vertical line. For definitions of periods t1, t2 and t4, see Materials and methods. (B) I2 kinematics in the second swallow. The second sequence from the images in set 7725 starts with image 45 and ends with image 67. The onset of the t4 period is frame 45, the onset of the t1 period is frame 53 and the onset of the t2 period is frame 63. (C) I2 kinematics in the third swallow. The first sequence from the images in set 7732 starts with image 16 and ends with image 39. The onset of the t4 period is frame 16, the onset of the t1 period is frame 26 and the onset of the t2 period is frame 35. (D) I2 kinematics in the fourth swallow, whose individual images are shown in Fig. 5. The second sequence from the images in set 7732 starts with image 39 and ends with image 60. The onset of the t4 period is frame 39, the onset of the t1 period is frame 47 and the onset of the t2 period is frame 56. (E) Normalized, averaged and smoothed I2 kinematics during swallowing cycle. Data are shown as the mean ± 1 S.D. (F) Normalized and averaged data from a transilluminated slug (replotted from Drushel et al., 1998) (the cycle starts at t4, and cycle length is renormalized to be the sum of the t4, t1 and t2 periods, excluding the t3 period). (G) Schematic diagrams indicating the length of I2 plotted in D for frames 1, 9, 18 and 22. I2 is highlighted with a black line. Compare original frames in Fig. 5.

View larger version (35K): [in a new window]   Fig. 8. Kinematics of the antero-posterior length of the I3 muscle during swallowing. (A-D) Data plotted as length (mm) as a function of time (ms). Left panels show the antero-posterior length of the I3 muscle on the dorsal surface. Right panels show the antero-posterior length of the I3 muscle on the ventral surface. (A) I3 kinematics in the first swallow. (B) I3 kinematics in the second swallow. (C) I3 kinematics in the third swallow. (D) I3 kinematics in the fourth swallow. (E) Normalized, averaged and smoothed anterio-posterior lengths of I3 during the swallowing cycle. Data are shown as mean ± 1 S.D. (F) Schematic diagrams indicating the antero-posterior length of I3 on the dorsal surface for frames 1, 9, 17, 18 and 22, highlighted with a black line. The antero-posterior lengths of I3 on the ventral surface for frames 1, 9, 18 and 22 are shown on the right, highlighted with a black line. Compare original frames in Fig. 5. For definitions of periods t1, t2 and t4, see Materials and methods.

View larger version (36K): [in a new window]   Fig. 9. Kinematics of the dorso-ventral length of the I3 muscle during swallowing. (A-D) Data from each of the four individual swallowing sequences plotted as length (mm) as a function of time (ms). The left panels show the dorso-ventral length of the I3 muscle at the lateral groove. The right panels show the dorso-ventral length of the I3 muscle at the line of the jaws. (E) Normalized, averaged and smoothed dorso-ventral lengths of I3 during the swallowing cycle. Data are shown as mean ± 1 S.D. (F) Schematic diagrams indicating the dorso-ventral length of I3 at the lateral groove for frames 1, 9, 18 and 22, highlighted with a black line. The dorso-ventral lengths of I3 at the jaws for frames 1, 9, 18 and 22 are shown on the right, highlighted with a black line. Compare original frames in Fig. 5. For definitions of periods t1, t2 and t4, see Materials and methods.

View larger version (18K): [in a new window]   Fig. 10. Overall movement of the buccal mass based on the changing angle of the jaw line relative to the fixed tank holding the animal. (A-D) Data from each of the four individual swallow sequences plotted as angle (degrees) as a function of time (ms). (E) Normalized, averaged and smoothed jaw line angle during the swallowing cycle. Data are shown as mean ± 1 S.D. Note that all four swallows show different patterns of change in the angle of the jaws. (F) A black line is used to highlight the jaw angle for frames 1, 9, 18 and 22. Compare original frames in Fig. 5. For definitions of periods t1, t2 and t4, see Materials and methods.

View larger version (35K): [in a new window]   Fig. 11. Movements of the odontophore relative to the buccal mass. The left panels show rotation of the anterior border of I6 relative to the jaw line. The right panels show translation of the anterior tip of the odontophore relative to the jaw line, with the jaw line rotated to be vertical. (A-D) The rotation (left panels, angle as a function of time) and translation [right panels, distance, in units of internal radular stalk width (RSW units) as a function of time] during each of the four individual swallowing sequences. (E) Normalized, averaged and smoothed rotations (left) and translations (right). Data are shown as the mean ± 1 S.D. (F) Schematic diagrams indicating the rotation of the odontophore for frames 1, 9, 18 and 22. The anterior margin of the odontophore is highlighted with a black line, and the jaw line (relative to which the angle is measured) is highlighted with a gray line. The translation of the odontophore for frames 1, 9, 18 and 22 is shown on the right. A gray line highlights the jaws, and a black line indicates the distance from the anteriormost point of the odontophore to the jaw line. Compare original frames in Fig. 5. For definitions of periods t1, t2 and t4, see Materials and methods.

View larger version (34K): [in a new window]   Fig. 12. Deformations of the odontophore during swallowing. To provide an internal reference frame for the odontophore, all measurements were made after the anterior border of I6 had been rotated so that it was vertical. All lengths in A—D are mm plotted as a function of time (ms). The left panels show the changes in the antero-posterior length; the right panels show the changes in the dorso-ventral length. (A—D) Data from each of the four individual swallowing sequences; (E) these data normalized, averaged and smoothed ± 1 S.D. (F) Schematic diagrams indicating the antero-posterior odontophore length for frames 1, 9, 18 and 22. The anterior margin of the odontophore is highlighted with a gray line, and a parallel line drawn at the maximum antero-posterior length is highlighted with a black line. The dorso-ventral lengths of the odontophore for frames 1, 9, 18 and 22 are shown on the right. A gray line highlights the anterior margin of the odontophore, and a black line indicates the maximum length in the dorso-ventral direction perpendicular to this reference line. Compare original frames in Fig. 5. For definitions of periods t1, t2 and t4, see Materials and methods.

View larger version (37K): [in a new window]   Fig. 13. Movements internal to the odontophore during swallowing. Measurements were made of the rotation of the radular stalk relative to the anterior border of muscle I6 (left panels) and the translation of the base of the radular stalk as a percentage of the dorso-ventral height of the odontophore (right panels). (A—D) Data from individual swallowing sequences. (E) These data normalized, averaged and smoothed ± 1 S.D. Angle (degrees) is plotted as a function of time (ms) in the left panels. Percentage of the odontophore height is plotted as a function of time (ms) in the right panels. (F) Schematic diagrams indicating the rotation of the radular stalk within the odontophore for frames 1, 9, 18 and 22. The anterior margin of the odontophore is highlighted with a gray line, and the line of the radular stalk is highlighted with a black line; the angle is measured relative to the gray line. The translation of the radular stalk for frames 1, 9, 18 and 22 is shown on the right. A gray line highlights the anterior margin of the odontophore, and a black line parallel to this line indicates the distance from the base of the radula to the base of the odontophore. Compare original frames in Fig. 5. For definitions of periods t1, t2 and t4, see Materials and methods.