First published online August 31, 2004
Journal of Experimental Biology 207, 3463-3476 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01140
Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray
Karen P. Maruska* and
Timothy C. Tricas
Department of Zoology and Hawai'i Institute of Marine Biology,
University of Hawai'i at Manoa, 2538 The Mall, Honolulu, HI 96822,
USA
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Fig. 1. The lateral line canal system on the dorsal (D) and ventral (V) surface of
the Atlantic stingray, Dasyatis sabina. Broken lines indicate
sections of canal that contain innervated neuromasts, while solid lines
represent neuromast-free tubules that terminate in pores. Neurophysiology
recordings were made from primary afferent neurons in the anterior lateral
line nerve that innervate neuromasts in the dorsal pored (Dp), ventral pored
(Vp), and ventral non-pored (Vnp) hyomandibular canals (HYO). Note that the
dorsal HYO contains numerous lateral tubules that branch to terminate in
pores, while the ventral hyomandibular canal contains a lateral pored section
and a medial non-pored section along the midline. IO, infraorbital canal; MAN,
mandibular canal; PLL, posterior lateral line canal; SO, supraorbital canal.
Scale bar, 1 cm. Modified from Maruska and Tricas
(1998 ).
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Fig. 2. Resting discharge patterns for individual primary afferent neurons that
innervate dorsal and ventral hyomandibular lateral line neuromasts in the
Atlantic stingray, Dasyatis sabina. Interspike interval (ISI)
histograms shown for individual neurons are representative of those recorded
from primary afferents in all canal subsystems. Irregular resting discharge
patterns were most common (45% of all units) and ISI distributions were
similar among dorsal and ventral primary afferents. Regular firing afferents
from ventral non-pored canals had slower discharge activity (greater ISI) than
those from dorsal pored canals. Histograms were calculated from 500
consecutive spikes and compiled in 2 ms bins. Discharge variability is
expressed as the coefficient of variation (CV), which is the dimensionless
ratio of S.D. to mean interspike interval.
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Fig. 3. Interspike interval (ISI) frequency histograms of primary afferent neurons
that innervate dorsal pored (Dp), ventral pored (Vp) and ventral non-pored
(Vnp) hyomandibular canal neuromasts in the Atlantic stingray, Dasyatis
sabina. Primary afferents that innervate Vnp canals show slower, more
variable resting rates than do units from Dp and Vp canals. Also,
approximately one-third of units in Vnp canals had no resting discharge (i.e.
were silent). These features of the non-pored lateral line primary afferents
are consistent with the idea of enhanced detection of transient or phasic
stimuli produced by prey. Sample sizes (N) show the number of
animals, number of primary afferents sampled.
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Fig. 4. Relationship between mean interspike interval (ISI) and coefficient of
variation (CV) for regular and irregular primary afferent neurons from dorsal
pored (Dp), ventral pored (Vp) and ventral non-pored (Vnp) canals in the
Atlantic stingray, Dasyatis sabina. Primary afferents with regular
discharge activity (Reg; closed symbols) have lower CV values than irregular
units (Irreg; open symbols) for all canal types. ISI values differ between
regular and irregular units for Dp and Vp, but not Vnp primary afferents.
Further, regular Dp afferents have higher CV and lower ISI values than regular
Vnp afferents. Data are plotted as mean ±
S.E.M.
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Fig. 5. Relationship between neural response at best frequency and stimulus
intensity for three representative primary afferent neurons from the dorsal
pored hyomandibular canal of the Atlantic stingray, Dasyatis sabina.
Relative neural gain varies among these units, but neural discharge
(peak–DC) increases as a linear function of stimulus intensity (re:
hydrodynamic acceleration estimated at the skin surface) for all three.
m, slope.
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Fig. 6. Bode plots for frequency responses to hydrodynamic and tactile stimuli for
primary afferent neurons that innervate lateral line canal neuromasts in the
dorsal pored (Dp), ventral pored (Vp) and ventral non-pored (Vnp)
hyomandibular canals of the Atlantic stingray, Dasyatis sabina.
Hydrodynamic stimuli: Dp primary afferents show peak frequency sensitivity at
20–90 Hz re: velocity (Ai) and a flat, relatively untuned response up to
about 40 Hz when expressed in terms of acceleration (Aii). Vp primary
afferents show flat to low-pass characteristics when expressed in terms of
both velocity (Bi; <70 Hz) and acceleration (Bii; <30 Hz). Variation
among units is likely due to low sample size for this group (N=9).
Tactile stimuli: Vnp primary afferents stimulated by tactile depression of the
skin show a relatively flat response up to 30 Hz re: velocity (Ci) and a
low-pass response re: acceleration (Cii) with a 6 dB drop in neural response
achieved by 5 Hz. Thus, primary afferents from pored canals respond to
hydrodynamic acceleration and units from ventral non-pored canals respond to
the velocity of canal fluid induced by skin depression. Data were normalized
to a relative value of 0 dB assigned to the best frequency for each neuron and
expressed as relative neural gain (dB). All data are plotted as mean ±
S.E.M. for each stimulus frequency relative
to velocity (Ai–Ci) and acceleration (Aii–Cii). Sample sizes
(N) represent the number of animals, number of primary afferents
sampled. Note that some error bars are obscured by symbols.
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Fig. 7. Phase diagrams for frequency responses of primary afferent neurons from
dorsal pored (Dp) and ventral non-pored (Vnp) hyomandibular canals in the
Atlantic stingray, Dasyatis sabina. Dp primary afferents show a low
frequency phase lead of about 180° (acceleration-sensitive), while Vnp
primary afferents show a low frequency phase lead of about 90°
(velocity-sensitive). Phase of the peak neural response is expressed in
degrees (mean ± S.E.M.) relative to
the peak displacement of the sphere. Sample sizes (N) show the number
of animals, number of primary afferents analyzed.
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Fig. 9. Increase in relative neural gain to tactile stimulation over hydrodynamic
flow for primary afferent neurons in the ventral non-pored hyomandibular canal
of the stingray, Dasyatis sabina. Mean tactile sensitivity of three
primary afferents from ventral non-pored canals (open circles) normalized
relative to their average response to hydrodynamic flow above the canal (solid
circles at 0 dB) across different stimulus frequencies are shown. Note that
the average neural response is 6–20 dB greater to direct tactile stimuli
compared to hydrodynamic stimuli above the canal, and are highest at the lower
frequencies (10–20 Hz). Thus, non-pored canals are an average of
2–10 times more sensitive to tactile stimuli than to local water
movements. Values are means ± S.E.M.
and error bars are shown only in the negative direction on the 0 dB line for
clarity. The broken line represents a relative neural gain of 6 dB.
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Fig. 10. Frequency distributions of hair cell orientations on lateral line canal
neuromasts in the Atlantic stingray, Dasyatis sabina. The main
neuromast and longitudinal canal axis lies along the 0–180° line
(inset). Semicircular (from 0–180°) angular orientations from the
canal axis are expressed as the percentage of total hair cells and compiled in
11.25° bins. Neuromasts in all three canal subsystems have the majority
(>85%) of hair cells oriented within 45° of the main canal axis, and a
small percentage oriented nearly orthogonal (90°) to this axis. However,
there are no differences in hair cell orientations among dorsal pored (Dp),
ventral pored (Vp) and ventral non-pored (Vnp) neuromasts. Sample sizes
(N) represent the number of animals, number of hair cells
measured.
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© The Company of Biologists Ltd 2004
5–10 Hz, while afferents from Dp canals respond best to
acceleration stimuli at