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Electrosensitive spatial vectors in elasmobranch fishes: implications for source localization.

Rivera-Vicente AC, Sewell J, Tricas TC - PLoS ONE (2011)

Bottom Line: The MAN canals of all species project in anterior or posterior directions behind the mouth and likely coordinate prey capture.Vertical elevation was greatest in the BUC of the sandbar shark, restricted by the hammerhead cephalofoil and extremely limited in the dorsoventrally flattened stingray.These results are consistent with the functional subunit hypothesis that predicts specialized ampullary functions for processing of weak dipole and geomagnetic induced fields, and provides an anatomical basis for future experiments on central processing of different forms of relevant electric stimuli.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America.

ABSTRACT
The electrosense of sharks and rays is used to detect weak dipole-like bioelectric fields of prey, mates and predators, and several models propose a use for the detection of streaming ocean currents and swimming-induced fields for geomagnetic orientation. We assessed pore distributions, canal vectors, complementarity and possible evolutionary divergent functions for ampullary clusters in two sharks, the scalloped hammerhead (Sphyrna lewini) and the sandbar shark (Carcharhinus plumbeus), and the brown stingray (Dasyatis lata). Canal projections were determined from measured coordinates of each electrosensory pore and corresponding ampulla relative to the body axis. These species share three ampullary groups: the buccal (BUC), mandibular (MAN) and superficial ophthalmic (SO), which is subdivided into anterior (SOa) and posterior (SOp) in sharks. The stingray also has a hyoid (HYO) cluster. The SOp in both sharks contains the longest (most sensitive) canals with main projections in the posterior-lateral quadrants of the horizontal plane. In contrast, stingray SO canals are few and short with the posterior-lateral projections subsumed by the HYO. There was strong projection coincidence by BUC and SOp canals in the posterior lateral quadrant of the hammerhead shark, and laterally among the stingray BUC and HYO. The shark SOa and stingray SO and BUC contain short canals located anterior to the mouth for detection of prey at close distance. The MAN canals of all species project in anterior or posterior directions behind the mouth and likely coordinate prey capture. Vertical elevation was greatest in the BUC of the sandbar shark, restricted by the hammerhead cephalofoil and extremely limited in the dorsoventrally flattened stingray. These results are consistent with the functional subunit hypothesis that predicts specialized ampullary functions for processing of weak dipole and geomagnetic induced fields, and provides an anatomical basis for future experiments on central processing of different forms of relevant electric stimuli.

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Directions of electrosensory canal projections relative to the shark body.(A) Projections originate along the central body axis and are anterior (A), dorsal (D) or lateral (L) relative to the body, with complementary posterior, ventral and medial projections, respectively (not illustrated). (B) Spherical projection vectors for each ampullary canal are expressed as direction relative to the shark body. Direction origins are at the ampulla and have projections relative to the anterior, dorsal or lateral direction of the body. Azimuth (θ, theta) is calculated as the angle of deviation from the anterior direction in the horizontal plane, and elevation (ϕ, phi) in the orthogonal vertical plane.
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pone-0016008-g001: Directions of electrosensory canal projections relative to the shark body.(A) Projections originate along the central body axis and are anterior (A), dorsal (D) or lateral (L) relative to the body, with complementary posterior, ventral and medial projections, respectively (not illustrated). (B) Spherical projection vectors for each ampullary canal are expressed as direction relative to the shark body. Direction origins are at the ampulla and have projections relative to the anterior, dorsal or lateral direction of the body. Azimuth (θ, theta) is calculated as the angle of deviation from the anterior direction in the horizontal plane, and elevation (ϕ, phi) in the orthogonal vertical plane.

Mentions: In marine sharks and rays the ampullae are organized into distinct subdermal groups or clusters that are associated with branches of the anterior lateral line nerve [28] to guide orientation behaviors. The ampullary canals radiate in different directions from these clusters to pores distributed widely over the head (and body of batoids) (Fig. 1). The spatial separation of each ampulla and its pore results in canal projections that are multidirectional with respect to the body axis of the animal and surrounding space. The spatial arrangement of the electrosensory array is an important determinant for localization of electric field sources, but the translation of complex field stimuli by the entire array complex in space is uncharacterized. Sharks may follow electric field lines from an external source by maintaining a constant representation of the field signature on the head, or alternatively may derive the source location by differential sampling across the electrosensory array [29]. Detailed studies of the orientation patterns to dipole electric stimuli show that there is great variation in approach paths of some sharks [30]. The somatotopic representation of these external fields results from characteristics of the array such as the number and position of clusters, number of ampullary canals, and the length and spatial projection of canals relative to the midline of the animal. For example, ampullae with long canals will sample a larger segment of a uniform electric field and their associated primary afferent neurons will receive proportionally more excitation (or inhibition) than ampullae with shorter canals. In addition, canals that are oriented parallel to uniform field lines will be maximally excited and those with orthogonal orientation will be insensitive [15], [31]. Recent work shows that the spatial projections of the skate hyoid array in two dimensions can enhance coding efficiency by the peripheral nervous system for a dipole stimulus [32]. Thus, characterization of the spatial organization of the electrosensory array is needed to develop realistic peripheral and central neural computation models.


Electrosensitive spatial vectors in elasmobranch fishes: implications for source localization.

Rivera-Vicente AC, Sewell J, Tricas TC - PLoS ONE (2011)

Directions of electrosensory canal projections relative to the shark body.(A) Projections originate along the central body axis and are anterior (A), dorsal (D) or lateral (L) relative to the body, with complementary posterior, ventral and medial projections, respectively (not illustrated). (B) Spherical projection vectors for each ampullary canal are expressed as direction relative to the shark body. Direction origins are at the ampulla and have projections relative to the anterior, dorsal or lateral direction of the body. Azimuth (θ, theta) is calculated as the angle of deviation from the anterior direction in the horizontal plane, and elevation (ϕ, phi) in the orthogonal vertical plane.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3020962&req=5

pone-0016008-g001: Directions of electrosensory canal projections relative to the shark body.(A) Projections originate along the central body axis and are anterior (A), dorsal (D) or lateral (L) relative to the body, with complementary posterior, ventral and medial projections, respectively (not illustrated). (B) Spherical projection vectors for each ampullary canal are expressed as direction relative to the shark body. Direction origins are at the ampulla and have projections relative to the anterior, dorsal or lateral direction of the body. Azimuth (θ, theta) is calculated as the angle of deviation from the anterior direction in the horizontal plane, and elevation (ϕ, phi) in the orthogonal vertical plane.
Mentions: In marine sharks and rays the ampullae are organized into distinct subdermal groups or clusters that are associated with branches of the anterior lateral line nerve [28] to guide orientation behaviors. The ampullary canals radiate in different directions from these clusters to pores distributed widely over the head (and body of batoids) (Fig. 1). The spatial separation of each ampulla and its pore results in canal projections that are multidirectional with respect to the body axis of the animal and surrounding space. The spatial arrangement of the electrosensory array is an important determinant for localization of electric field sources, but the translation of complex field stimuli by the entire array complex in space is uncharacterized. Sharks may follow electric field lines from an external source by maintaining a constant representation of the field signature on the head, or alternatively may derive the source location by differential sampling across the electrosensory array [29]. Detailed studies of the orientation patterns to dipole electric stimuli show that there is great variation in approach paths of some sharks [30]. The somatotopic representation of these external fields results from characteristics of the array such as the number and position of clusters, number of ampullary canals, and the length and spatial projection of canals relative to the midline of the animal. For example, ampullae with long canals will sample a larger segment of a uniform electric field and their associated primary afferent neurons will receive proportionally more excitation (or inhibition) than ampullae with shorter canals. In addition, canals that are oriented parallel to uniform field lines will be maximally excited and those with orthogonal orientation will be insensitive [15], [31]. Recent work shows that the spatial projections of the skate hyoid array in two dimensions can enhance coding efficiency by the peripheral nervous system for a dipole stimulus [32]. Thus, characterization of the spatial organization of the electrosensory array is needed to develop realistic peripheral and central neural computation models.

Bottom Line: The MAN canals of all species project in anterior or posterior directions behind the mouth and likely coordinate prey capture.Vertical elevation was greatest in the BUC of the sandbar shark, restricted by the hammerhead cephalofoil and extremely limited in the dorsoventrally flattened stingray.These results are consistent with the functional subunit hypothesis that predicts specialized ampullary functions for processing of weak dipole and geomagnetic induced fields, and provides an anatomical basis for future experiments on central processing of different forms of relevant electric stimuli.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America.

ABSTRACT
The electrosense of sharks and rays is used to detect weak dipole-like bioelectric fields of prey, mates and predators, and several models propose a use for the detection of streaming ocean currents and swimming-induced fields for geomagnetic orientation. We assessed pore distributions, canal vectors, complementarity and possible evolutionary divergent functions for ampullary clusters in two sharks, the scalloped hammerhead (Sphyrna lewini) and the sandbar shark (Carcharhinus plumbeus), and the brown stingray (Dasyatis lata). Canal projections were determined from measured coordinates of each electrosensory pore and corresponding ampulla relative to the body axis. These species share three ampullary groups: the buccal (BUC), mandibular (MAN) and superficial ophthalmic (SO), which is subdivided into anterior (SOa) and posterior (SOp) in sharks. The stingray also has a hyoid (HYO) cluster. The SOp in both sharks contains the longest (most sensitive) canals with main projections in the posterior-lateral quadrants of the horizontal plane. In contrast, stingray SO canals are few and short with the posterior-lateral projections subsumed by the HYO. There was strong projection coincidence by BUC and SOp canals in the posterior lateral quadrant of the hammerhead shark, and laterally among the stingray BUC and HYO. The shark SOa and stingray SO and BUC contain short canals located anterior to the mouth for detection of prey at close distance. The MAN canals of all species project in anterior or posterior directions behind the mouth and likely coordinate prey capture. Vertical elevation was greatest in the BUC of the sandbar shark, restricted by the hammerhead cephalofoil and extremely limited in the dorsoventrally flattened stingray. These results are consistent with the functional subunit hypothesis that predicts specialized ampullary functions for processing of weak dipole and geomagnetic induced fields, and provides an anatomical basis for future experiments on central processing of different forms of relevant electric stimuli.

Show MeSH