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Link to original content: https://pubmed.ncbi.nlm.nih.gov/33791526
Eye Movements in Frogs and Salamanders-Testing the Palatal Buccal Pump Hypothesis - PubMed Skip to main page content
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. 2019 Jun 7;1(1):obz011.
doi: 10.1093/iob/obz011. eCollection 2019.

Eye Movements in Frogs and Salamanders-Testing the Palatal Buccal Pump Hypothesis

Affiliations

Eye Movements in Frogs and Salamanders-Testing the Palatal Buccal Pump Hypothesis

F Witzmann et al. Integr Org Biol. .

Abstract

In frogs and salamanders, movements of the eyeballs in association with an open palate have often been proposed to play a functional role in lung breathing. In this "palatal buccal pump," the eyeballs are elevated during the lowering of the buccal floor to suck air in through the nares, and the eyeballs are lowered during elevation of the buccal floor to help press air into the lungs. Here, we used X-Ray Reconstruction of Moving Morphology to investigate eye movements during lung breathing and feeding in bullfrogs and axolotls. Our data do not show eye movements that would be in accordance with the palatal buccal pump. On the contrary, there is a small passive elevation of the eyeballs when the buccal floor is raised. Inward drawing of the eyeballs occurs only during body motion and for prey transport in bullfrogs, but this was not observed in axolotls. Each eye movement in bullfrogs has a vertical, a mediolateral, and an anteroposterior component. Considering the surprisingly weak posterior motion component of the eyeballs, their main role in prey transport might be fixing the prey by pressing it against the buccal floor. The retraction of the buccal floor would then contribute to the posterior push of the prey. Because our study provides no evidence for a palatal buccal pump in frogs and salamanders, there is also no experimental support for the idea of a palatal buccal pump in extinct temnospondyl amphibians, in contrast to earlier suggestions.

Augenbewegungen bei Fröschen und Salamandern-Prüfung der “palatalen Bukkalpumpen”-Hypothese Bei Fröschen und Salamandern wurde oft vorgeschlagen, dass Bewegungen der Augäpfel in Verbindung mit einem offenen Gaumen eine funktionale Rolle bei der Lungenatmung spielen. Bei dieser “palatalen Bukkalpumpe” werden die Augäpfel während des Absenkens des Mundbodens angehoben, um Luft durch die Nasenlöcher anzusaugen, und die Augäpfel werden während des Anhebens des Mundbodens abgesenkt, um Luft in die Lungen zu drücken. Hier verwendeten wir Röntgenrekonstruktionen der Bewegungsmorphologie, um Augenbewegungen während der Lungenatmung und bei der Ernährung von Ochsenfröschen und Axolotl zu untersuchen. Unsere Daten zeigen keine Augenbewegungen, die der palatalen Bukkalpumpe entsprechen würden. Im Gegenteil, es gibt eine kleine passive Anhebung der Augäpfel, wenn der Mundboden angehoben wird. Ein nach innen Ziehen der Augäpfel tritt nur während der Körperbewegung und für den Beutetransport in Ochsenfröschen auf, bei Axolotl wurde dies jedoch nicht beobachtet. Jede Augenbewegung in Ochsenfröschen hat eine vertikale, eine mediolaterale und eine anteroposteriore Komponente. Angesichts der überraschend schwachen posterioren Bewegungskomponente der Augäpfel könnte ihre Hauptaufgabe beim Beutetransport die Fixierung der Beute sein, indem sie gegen den bukkalen Mundboden Boden gedrückt wird. Das Zurückziehen des Mundbodens würde dann zum nach hinten gerichteten Schub der Beute beitragen. Da unsere Studie keine Belege für eine palatale Bukkalpumpe in Fröschen und Salamandern liefert, gibt es im Gegensatz zu früheren Vorschlägen auch keine experimentelle Unterstützung für die Idee einer palatalen Bukkalpumpe in ausgestorbenen temnospondylen Amphibien. translated to German by F. Klimm (frederike.klimm@neptun.uni-freiburg.de).

حركات العين في الضفادع والسمندل - اختبار فرضية مضخة الشدق الحنكي في الضفادع والسمندل، غالبًا ما يُقترح حركات مقل العيون المرتبطة بالحنك المفتوح للعب دور وظيفي في التنفس الرئوي. في "مضخة الشدق الحنكي" هذه، يتم رفع مقل العيون خلال خفض أرضية الشدق لامتصاص الهواء من خلال فتحتي الأنف، ويتم إنزال مقل العيون أثناء ارتفاع أرضية الشدق للمساعدة في ضغط الهواء داخل الرئتين. استخدمنا هنا X-Ray Reconstruction of Moving Morphology للتحقيق في حركات العين أثناء التنفس الرئوي والتغذية في الضفادع وعفريت الماء. لا تُظهر بياناتنا توافق حركات العين مع مضخة الشدق الحنكية. على العكس من ذلك، هناك ارتفاع سلبي صغير في مقل العيون عند رفع أرضية الشدق. يحدث مد داخلي للعينين فقط أثناء حركة الجسم ونقل الفرائس في الضفادع، ولكن هذا لم يلاحظ في عفريت الماء. تحتوي كل حركة عين في الضفادع على عنصر رأسي، ومتوسط جانبي، ومكون أمامي خلفي. بالنظر إلى مكون الحركة الخلفية الضعيفة بشكل مدهش في مقل العيون، فإن دورها الرئيسي في نقل الفرائس قد يكون تلصيق الفريسة عن طريق الضغط عليها ضد أرضية الشدق. وسيسهم تراجع أرضيه الشدق في الدفع الخلفي للفريسة. نظرًا لأن دراستنا لا تقدم أي دليل على وجود مضخة شدقية حنكية في الضفادع والسمندل، لا يوجد أيضًا أي دعم تجريبي لفكرة مضخة شدقية حنكية في البرمائيات Temnospondyli المنقرضة، على عكس الاقتراحات السابقة. translation by A.A. Elbassiouny ( ahmed.elbassiouny@utoronto.ca ).

Movimientos oculares en ranas y salamandras: prueba de la hipótesis de la bomba bucal palatina (Eye movements in frogs and salamanders – testing the palatal buccal pump hypothesis) En ranas y salamandras, los movimientos oculares asociados con el paladar abierto a menudo se ha propuesto que desempeñan un papel funcional en la respiración pulmonar. En esta “bomba bucal palatina”, los globos oculares se elevan durante la bajada del piso bucal para inhalar por las narinas, y los globos oculares se bajan durante la elevación del piso bucal para ayudar a presionar el aire hacia los pulmones. Aquí utilizamos la Reconstrucción de Rayos X de la Morfología en Movimiento para investigar los movimientos oculares durante la respiración pulmonar y la alimentación en ranas mugidoras y ajolotes. Nuestros datos no muestran movimientos oculares que estarían de acuerdo con la bomba bucal palatina. Por el contrario, hay una pequeña elevación pasiva de los globos oculares cuando se eleva el suelo bucal. La retracción interna de los globos oculares ocurre solo durante el movimiento del cuerpo y para el transporte de presas en las ranas mugidoras, pero esto no se observó en los ajolotes. Cada movimiento ocular en las ranas mugidoras tiene un componente vertical, mediolateral y anteroposterior. Considerando el componente de movimiento posterior sorprendentemente pequeño de los globos oculares, su función principal en el transporte de presas podría ser la fijación de la presa presionándola contra el suelo bucal. La retracción del suelo bucal contribuiría entonces al empuje posterior de la presa. Debido a que nuestro estudio no proporciona evidencia de una bomba bucal palatina en ranas y salamandras, tampoco hay apoyo experimental para la idea de una bomba bucal palatina en anfibios temnospóndilos extintos, en contraste con sugerencias anteriores. translated to Spanish by Y.E. Jimenez (yordano_jimenez@brown.edu).

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Figures

Fig. 1
Fig. 1
Palate of a frog (Rana sp.) showing the associated muscles in ventral view after removal of the buccal mucosa (redrawn and modified after Gaupp 1904). In the morphological left interpterygoid vacuity, the m. levator bulbi and the Harderian gland have been removed. ch, choana; eb, eyeball; fit, fascia infratemporalis; hg, Harderian gland; iptv, interpterygoid vacuity; lc, lamina cribrosa; mLB, m. levator bulbi; mOI, m. obliquus inferior; mRB, m. retractor bulbi; mRI, m. rectus inferior; mRL, m. rectus lateralis; mRM, m. rectus medialis; msa, membrana subocularis anterior; msp, membrana subocularis posterior; pal, palatine; ps-bp, basal plate of parasphenoid; ps-pc, cultriform process of parasphenoid; pt, pterygoid; sph, sphenethmoid; vo, vomer.
Fig. 2
Fig. 2
Simplified cladogram of early tetrapod relationships after Ruta and Coates (2007). Palates drawn after Romer and Witter (1942), Beaumont (1977), Reisz (1977), Duellman and Trueb (1994), Laurin (1996), Schoch and Milner (2000), Sigurdsen and Bolt (2010), and Clack (2012).
Fig. 3
Fig. 3
Positions of the bone and muscle markers and of the ACS in the bullfrog and the axolotl. (AC) Bullfrog (Lc01). (A) Skull in dorsal view showing the markers in the bones (green), in the m. levator bulbi ventral to the eyes (red) and in the buccal floor (blue). (B) Left lateral view of same specimen as in (A). (C) Skull with attached ACS in left lateral view. (DF) Axolotl (Am03). (D) Skull in dorsal view showing the markers in the bones (green), in the m. levator bulbi ventral to the eyes (red) and in the buccal floor (blue). (E) Left lateral view of same specimen as in (D). (F) Skull with attached ACS in left lateral view. bm, marker in buccal floor (m. geniohyoideus); em, marker in orbital floor (m. levator bulbi); fpm, marker in frontoparietal bone; mm, marker in maxillary bone; nm, marker in nasal bone; otm, marker in otic capsule; pm, marker in parietal bone; pmm, marker in premaxillary bone; ptm, marker in pterygoid bone; smd, marker in dorsal part of squamosal bone; smv, marker in ventral part of squamosal bone.
Fig. 4
Fig. 4
Elevation and depression of the eyes and buccal floor during buccal oscillation, lung ventilation, and body movement in a bullfrog. Upward deflection of the motion traces is elevation and downward deflection is depression. The buccal floor elevates and both eyes depress during body movement. osc, buccal oscillation; breath, buccal pump for lung ventilation.
Fig. 5
Fig. 5
Eye translations in 3D during body motion in bullfrogs. (A) Example trace with inset of the ACS. Eye depression in blue, medial motion in green, and retraction in red. (B) Percentage of the total motion from each translational degree of freedom.
Fig. 6
Fig. 6
Depression of the left eye and elevation and retraction of the buccal floor during prey (cricket) transport in a bullfrog. Upward deflection of the motion traces is elevation or protraction and downward deflection is depression or retraction.
Fig. 7
Fig. 7
Eye and buccal floor motions during an air gulp in an axolotl. A slight preparatory phase of buccal floor elevation and protraction produces slight elevation of the eyes. The eyes do not move in any consistent manner during the air gulp.
Fig. 8
Fig. 8
Eye and buccal floor motions during suction feeding and prey (cricket) processing in an axolotl. The eyes depress slightly (<1 mm) during the suction strike, and then move slightly and inconsistently during prey processing. Note the different scales for eye (left axis) and buccal motions (right axis).

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