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First published online January 8, 2007
Journal of Experimental Biology 210, 238-260 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02654

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The kinematics of multifunctionality: comparisons of biting and swallowing in Aplysia californica

David M. Neustadter^1,*, Robert L. Herman², Richard F. Drushel³, David W. Chestek¹ and Hillel J. Chiel^3,4,1,

¹ Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH 44106, USA
² Department of Electrical Engineering and Computer Science, Case Western Reserve University, Cleveland, OH 44106, USA
³ Department of Biology, Case Western Reserve University, Cleveland, OH 44106, USA
⁴ Department of Neurosciences, Case Western Reserve University, Cleveland, OH 44106, USA

View larger version (51K): [in this window] [in a new window]   Fig. 1. Anatomy of the buccal mass, and revision of jaw line measurement. (A) Mid-sagittal anatomy of the buccal mass, based on a formaldehyde-fixed hemi-sectioned buccal mass. (B) External oblique view of dissected buccal mass, showing location of jaw line (lines labeled `Line of jaws'). The I1/I3/jaw complex extends antero-posteriorly from the lateral groove to the jaw line. (C) Line marked `previous' indicates the jaw line used in previous work (Neustadter et al., 2002a). Line marked `revised' is drawn from the dorsal point of inflection of the jaw cartilage, which appears as a dark region, to the ventral point of inflection of the jaw cartilage. This more accurately reflects both the external and internal anatomy of the jaw cartilage, which appears in the MR image as a dark region. (D) Antero-posterior views of three-dimensional kinematic model during swallowing using the new jaw line. Blue mesh represents the I1/I3/jaw complex, yellow mesh represents the odontophore, and red solid represents the radular stalk. (1) Transition, (2) protraction, (3) retraction. These views are based on frames 17, 24, and 35, respectively, of sequence 7732-S3. Compare with the bottom row of fig. 11 in Neustadter et al. (Neustadter et al., 2002b). The revised jaw line generates images that are more similar to those observed during swallowing in vivo.

View larger version (53K): [in this window] [in a new window]   Fig. 2. Schematic summary of the movements of the entire buccal mass during a biting cycle. This summary is based on the data presented in this paper and incorporates observations from in vivo high-temporal-resolution MR images in intact, behaving animals as well as high-spatial-resolution MR images of anesthetized buccal masses. Details not visible in the MR images are based on observations of buccal masses or isolated odontophores undergoing pharamacologically induced feeding-like movements, as well as from dissections of fresh and fixed buccal masses. All illustrations are in orthographic projection. (A) Row shows a superficial lateral view of the outer buccal mass. Fiber directions of the thin, overlying I1 muscle are schematically indicated (see Fig. 12A). (B) Row shows a mid-sagittal view. (C) Row shows a dorsal view. The upper half of each panel shows a superficial dorsal view, whereas the lower half shows a view in which the radular surface and the I4 muscles are transparent, revealing the ventral structures beneath them. Columns 1-6 correspond to frames 53, 56, 60, 63, 68, 71 of sequence 3222 (respectively). The circumferential muscle shown in C2 was designated as such by Starmühlner (Starmühlner, 1956). The nomenclature for the other intrinsic muscles (I1 through I10) follows Howells (Howells, 1942) and Evans et al. (Evans et al., 1996), and the nomenclature for the extrinsic muscles (E1-E3 and E6) follows Chiel et al. (Chiel et al., 1986) and Howells (Howells, 1942). Compare with fig. 21 of Neustadter et al. (Neustadter et al., 2002b).

View larger version (98K): [in this window] [in a new window]   Fig. 3. A sequence of magnetic resonance (MR) images showing biting in response to a rapidly withdrawn piece of seaweed. Frames are acquired in 155 ms and are separated by 310 ms. The high temporal resolution data are shown above the kinematic measures taken from these images (see Materials and methods). This sequence is 3213, frames 26-43.

View larger version (68K): [in this window] [in a new window]   Fig. 4. Three-dimensional kinematic model of the buccal mass during a biting cycle. The I1/I3 muscles are shown as a continuous blue mesh, the odontophore is shown as a continuous yellow mesh, and the radular stalk is shown as a red solid. Views are shown in orthographic projection. (A) Right lateral views of transition, protraction and retraction. The central panel shows a side view of protraction; the arrows to the left indicate the contact between the posterior I3 muscle and the posterior of the radula/odontophore. The arrow to the right indicates a gap between the dorsal surface of the odontophore and the dorsal portion of the anterior I3 muscle; compare the views shown in Fig. 12D,E. (B) Dorso-ventral views of transition, protraction and retraction. The lateral groove (posteriormost edge of the I1/I3/jaw complex) has been rotated so that it is vertical. (C) Antero-posterior views of transition, protraction and retraction. The left, middle and right columns are based on frames 26, 34 and 39, respectively, of bite 3213. Compare with fig. 11 of Neustadter et al. (Neustadter et al., 2002b).

View larger version (19K): [in this window] [in a new window]   Fig. 5. Kinematics of the I2 muscle during biting versus swallowing. (A-D) Data from individual bites are shown to indicate the variability in individual responses. In all subsequent figures, only averaged data are shown. Data in A-D are plotted as length (mm) as a function of time (ms). (A) I2 kinematics in the first bite. This sequence from 7725 begins with frame 2 and ends with frame 25. The onset of the t1 period (see Materials and methods) is frame 13. (B) I2 kinematics in the second bite. This sequence from 3213 begins with frame 26 and ends with frame 43. The onset of the t1 period is frame 34. (C) I2 kinematics in the third bite. This sequence from 3213 begins with frame 43 and ends with frame 60. The onset of the t1 period is frame 49. (D) I2 kinematics in the fourth bite. This sequence from 3222 begins with frame 53 and ends with frame 72. The onset of the t1 period is frame 61. (E) Averaged data normalized to total cycle length. Lengths are not normalized. Values are means (solid lines) ± 1 s.d. (broken lines). Black lines, averaged data from biting responses; gray lines, averaged data from swallowing responses [data for swallowing in this and all subsequent figures are from Neustadter et al. (Neustadter et al., 2002a), re-analyzed using the new jaw line as described in Materials and methods]. Black vertical line represents the average t4/t1 border for the averaged bite data; gray vertical lines represent the average t4/t1 and t1/t2 borders for the averaged swallow data. (F) Schematic diagrams indicating the I2 length plotted in A for frames 1, 12, 19 and 24. Muscle I2 is highlighted with a black line.

View larger version (47K): [in this window] [in a new window]   Fig. 6. Kinematics of the antero-posterior and dorso-ventral length of the I1/I3/jaw complex during biting versus swallowing. (A,C) Averaged antero-posterior length along the dorsal surface (A) or the ventral surface (C) during biting or swallowing, shown using black or gray lines, respectively. (E,G) Averaged dorso-ventral length at the lateral groove (E) or at the jaw line (G) during biting or swallowing, shown using black or gray lines, respectively. Values are means (solid lines) ± 1 s.d. (broken lines). (B,D,F,H) Schematic diagrams showing the lengths (bold lines) measured to generate these averages for the frames indicated in Fig. 5 through the biting cycle.

View larger version (23K): [in this window] [in a new window]   Fig. 7. Estimates of the kinematics of the medio-lateral widths of the I3 muscle during biting using the three-dimensional kinematic model. A schematic medio-lateral view of the I1/I3/jaw complex is shown in Fig. 2C. (A-D) Widths of the continuous mesh representing the I3 muscle at six evenly spaced locations along its antero-posterior length for the first to fourth bites. The top trace in each panel (solid black line) is the medio-lateral width of the I3 muscle at the lateral groove. The bottom trace in each panel (broken line) is the medio-lateral width of the I3 muscle at the jaws.

View larger version (20K): [in this window] [in a new window]   Fig. 8. Movements of the odontophore relative to the buccal mass during biting versus swallowing. (A) Biting (black lines) and swallowing (gray lines) data showing averaged rotation of the anterior border of the I6 relative to the jaw line (black and gray lines, respectively, in (B). (C) Biting (black lines) and swallowing (gray lines) data showing translation of the anterior tip of the odontophore relative to the jaw line (black and gray lines, respectively, in (D). In C, the gray horizontal line indicates the location of the jaws (corresponding to 0 mm). When the data lie above this line, the radula and underlying odontophore are protruding through the jaws. Note that the averaged swallows do not cross this line, whereas the averaged bites do cross it. Values in A and C are means (solid lines) ± 1 s.d. (broken lines).

View larger version (26K): [in this window] [in a new window]   Fig. 9. Antero-posterior, dorso-ventral and medio-lateral dimensions of the odontophore during biting versus swallowing. Measurements were made after the anterior border of I6 had been rotated so that it was vertical. Averaged antero-posterior (A) and dorso-ventral (C) odontophore length normalized to cycle time; black lines are for biting, gray lines are for swallowing. (B,D) Schematic diagrams of lengths measured. (E) Medio-lateral half-widths in biting versus swallowing estimated from the kinematic model. A schematic medio-lateral view of the odontophore is shown in Fig. 2C. The half-width is reported, since this is likely to approximate the medio-lateral extent of the horseshoe-shaped I4 muscle (each half of which underlies the radula). Values in A, C and E are means (solid lines) ± 1 s.d. (broken lines).

View larger version (31K): [in this window] [in a new window]   Fig. 10. Movements of the radular stalk relative to the odontophore during biting versus swallowing. (A-D) Averaged rotation (A) and translation (C) of the radular stalk (black lines are for biting, gray lines for swallowing). Measurements were made of the rotation of the radular stalk relative to the anterior border of muscle I6 (in B, the line of the radular stalk is highlighted with a black line, and the anterior border of muscle I6 is highlighted with a gray line), and the translation of the base of the radular stalk relative to the dorso-ventral height of the odontophore (in D, the distance from the base of the radular stalk to the base of the odontophore is highlighted with a black line). In C, the horizontal gray line indicates when the base of the radular stalk is exactly coincident with the base of the odontophore. When the data lie above this line, the radular stalk has moved towards the dorsal surface of the odontophore; when the data lie below this line, the radula stalk is protruding ventrally out of the odontophore. Values in A and C are means (solid lines) ± 1 s.d. (broken lines). (E,F) Model outputs of the peak of swallowing (E, 7732, S3, frame 26) and the peak of biting (F, 3213, S1, frame 34), to directly compare the positions of the radular stalk near the peak of protraction. The outlines of the radula/odontophore have been rotated so that the prow is straight, and lateral views are shown. Note that the radular stalk is closer to the top of the radula/odontophore at the peak protraction of biting (F) than at the peak protraction of swallowing (E).

View larger version (4K): [in this window] [in a new window]   Fig. 11. Estimates of the kinematics of the I7 muscle during biting using the three-dimensional kinematic model. A schematic view of the I7 muscle during a biting cycle is shown in Fig. 2B. Averaged lengths are normalized to the cycle times; black lines are for biting, gray lines are for swallowing. Values are means (solid lines) ± 1 s.d. (broken lines).

View larger version (71K): [in this window] [in a new window]   Fig. 12. External and internal anatomy of the I1/I3/jaw complex, and measurement of the circumference of the jaw cartilage during a bite. (A) Fiber directions in the I1 muscle visualized by staining with hematein (see Materials and methods). White lines have been added that closely follow discrete I1 fibers. A schematic view of fiber positions during the biting cycle is shown in Fig. 2A. (B) Fiber directions in the I3 muscle visualized by staining with Fast Green (see Materials and methods). Two white lines have been added that closely follow discrete I3 bands. (C) Dissected view of jaw cartilage within the I1/I3/jaw complex. Lines point to folds in the cartilage of the jaw. Note that the jaw cartilage only occupies approximately half of the full antero-posterior length of the I1/I3/jaw complex both dorsally and ventrally. Scale bar (1 cm) applies to A-C. (D-G) Measurement of circumference of jaw cartilage during a bite. Images are oriented so that the dorsal surface of the animal is at the top, as in Figs 1 and 2. Compare with the line drawings in fig. 2A of Morton and Chiel (Morton and Chiel, 1993a). (D) Circumference at peak protraction; the radula has just closed. Arrow indicates the dorsal region of the jaws that are not in contact with the dorsal surface of the radula. (E) Circumference just after peak protraction, as radula begins to rotate and retract posteriorly into the buccal cavity (0.5 s after image shown in D; arrow indicates the dorsal region of the jaws that is not in contact with the dorsal surface of the radula). (F) Circumference at the onset of folds in the cartilage (folds are indicated by arrows; 1.0 s after image shown in D). (G) Circumference as the jaws close (1.3 s after image shown in D).

View larger version (28K): [in this window] [in a new window]   Fig. 13. Estimate of forces of I1/I3/jaw complex on odontophore. (A) Graph of estimated net forces for successive frames of sequence 3213, images 26-43. See Materials and methods for description of force calculation. Nominal model force units are plotted against time (ms). Positive force values imply that the odontophore will be protracted; negative force values imply that the odontophore will be retracted. The four lines are plotted using the assumption that the ratio of force in the anterior half to the posterior half of the I1/I3/jaw muscle complex is 0.0 (top line), 0.3 (second from top), 0.6 (third from top), or 1.0 (bottom line). Whenever the data for different force ratios lies above the zero line (as it does for ratios of 0.3 and 0.0), this indicates that the structures are kinematically configured such that with this differential excitation ratio, the I3 muscle can function as a protractor. (B) Three-dimensional model right lateral views of the I1/I3/jaw complex (blue mesh) and odontophore (yellow solid), corresponding to the arrows above A (images 31, 33 and 35, respectively). Top row: I1/I3/jaw complex and odontophore. Bottom row: odontophore alone. In the center top image, the antero-dorsal I1/I3 mesh is not in contact with the dorsal surface of the odontophore, but it is in contact with the dorsal surface of the posterior part of the odontophore. Also note that, in the central bottom image, the posterior part of the odontophore widens towards its midpoint. (C) Three-dimensional model dorso-ventral views of the I1/I3/jaw complex corresponding to the arrows above A (images 31, 33 and 35, respectively). Top row: I1/I3/jaw complex and odontophore. Bottom row: odontophore alone. In the center top image, note that the posterior I1/I3 mesh is in contact with the posterior surface of the odontophore. In the center bottom image, note that the posterior part of the odontophore widens towards its midpoint.

View larger version (18K): [in this window] [in a new window]   Fig. 14. (A,B) Schematic representation of neural and muscular activations during biting and swallowing cycles. Extracellular recordings from nerve and muscle in intact, behaving animals were scanned from several different sources. Simultaneous recording from BN2 and RN were taken from Morton and Chiel (Morton and Chiel, 1993a). Simultaneous recordings from BN1, BN2 and BN3 were taken from unpublished observations (D. W. Morton and H. J. Chiel). Simultaneous recordings from I2 and from BN2 were taken from Hurwitz et al. (Hurwitz et al., 1996). Extracellular recordings from I5 (ARC) were taken from Cropper et al. (Cropper et al., 1990b), and were aligned with BN3 activity (which carries the axons of the B15/B16 motor neurons). Recordings from I10 (which are representative of activity in 17, I8, I9 and I10) were taken from Evans et al. (Evans et al., 1996). The lengths of the scanned recordings were scaled relative to one another using the duration of the opening of the jaws to the closing of the jaws during a bite, and aligned by peak protraction. Boxes were then drawn around the resulting extracellular recordings, providing a schematic representation of the relative sizes of the extracellular units and their timing relative to one another. The data in the swallowing part of the figure are based on fig. 20 of Neustadter et al. (Neustadter et al., 2002b). (C) Schematic representation of roles of motor neurons and multi-action neuron B4/B5 in controlling the transition from biting to swallowing. During biting, activity in the B4/B5 neurons is reduced [(Warman and Chiel, 1995); B4/B5 are shaded]. During swallowing, activity in the B4/B5 neurons increases (Warman and Chiel, 1995), inhibiting the onset of activity in the motor neurons for the I1/I3/jaw complex, B10, B6, B3 and B9 (Gardner, 1993).