Biol. Bull.
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Biol. Bull. 205: 216-218. (October 2003)
© 2003 Marine Biological Laboratory

Neural Recordings From the Lateral Line in Free-Swimming Toadfish, Opsanus tau

L. M. Palmer1,2, B. A. Giuffrida2 and A. F. Mensinger1,2

1 University of Minnesota, Duluth, MN
2 Marine Biological Laboratory, Woods Hole, MA

Fish and aquatic amphibians have evolved a unique lateral line system that detects local water displacements. The lateral line functions in surface feeding, rheotaxis, localization of underwater objects, and subsurface prey detection (1). The detection of biologically relevant stimuli must often be accomplished during reafferent stimulation from self-generated motion (swimming, ventilation). However, due to the constraints of conventional recording techniques, the activity of the lateral line during movement is difficult to quantify.

The development of an inductive telemetry system (2) enables neural activity to be recorded from free-swimming fish. The system utilizes inductive telemetry to transmit biological information from the fish to an external recording device. Consequently, fish are free from constraints and are able to behave in a quasi-natural environment. Using this technique, we investigated the activity of primary afferent fibers of the anterior lateral line nerve during self-induced motion in the oyster toadfish, Opsanus tau. Adult toadfish (28 ± 1.4 SE cm standard length, 675 ± 46 SE g) of either sex were lightly anesthetized in 0.001% tricaine (Sigma) and lightly paralyzed with pancuronium bromide (Sigma) (600 µg/kg). A microwire electrode was inserted into the dorsal ramus of the anterior lateral line nerve, which innervates the supraorbital and infraorbital lateral line (3). Once spontaneous or evoked activity of 1 to 3 afferent fibers was obtained, the electrode was attached to a cylindrical telemetry tag (15 mm diameter x 38 mm length) and mounted externally on the dorsal surface of the fish. The rechargeable telemetry tag was inductively coupled to a bimodal recording stage (45 cm diameter). The stage acts passively to receive the inductive telemetry signal and actively to produce the magnetic field necessary to recharge the capacitors on the tag. The fish is free to move throughout the aquarium; however, data acquisition and tag charging are only possible when the fish remains on or near the stage. Fish were placed on the stage in an experimental tank (1.6 m diameter, 20 cm water depth), and allowed to recover from the surgical procedure for at least 3 h before experiments were conducted.

Fish movement was monitored with a digital camera (30 frames/s) and correlated with nerve firing offline (ADInstruments, Chart4; Cambridge Electronic Designs, Spike2). Spontaneous neural activity was recorded in each fiber and correlated with ventilation cycles. Nerve firing was also recorded when the fish moved independently or was provoked into swimming by gently prodding its caudal fin with a rod. All swimming events consisted of short swimming bursts that displaced the fish up to a body length forward. Swimming speeds (range: 3.6–15.1 cm/s) were determined by videotape analysis.

The primary afferents of the anterior lateral line in the toadfish increased firing in response to swimming and ventilatory movements. During forward swimming, the firing rate of the anterior lateral line increased above spontaneous rates (Fig. 1A), and neural activity returned to spontaneous rate within 2 s. There was no correlation (r2 <= 0.07) between swimming speed and firing rate, suggesting that firing was saturated at all swimming events. This contrasted with previous work that indicates lateral line afferent activity is reduced during vigorous body movement (4). Anterior lateral line afferents were also stimulated by ventilatory movements (Fig. 1B). The responses of 15 (6 silent and 9 spontaneously active) fibers to the ventilatory cycle were monitored. Three silent fibers and three spontaneously active fibers fired in correlation with the exhalation phase of the ventilation cycle. The other nine fibers were not modulated by ventilation; however, we were unable to determine whether this was due to the distant location of the neuromast from the operculum or to efferent inhibitory activity.



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  		Figure 1. Neural activity of the anterior lateral line in Opsanus tau in response to reafferent self-generated motion. (A) The response of two fibers to short-range swimming events. The dashed black line represents the spontaneous activity of each fiber. The solid black line represents a linear regression through all data points (upper: y = -5.5x + 158.4, r2 = 0.07; lower: y = -0.9x + 58.3, r2 = 0.02). (B) Neural trace of a silent fiber (i.e., fiber with no spontaneous activity) that was responsive to the ventilation cycle. The fiber innervated a neuromast located on the infraorbital canal line. Arrows indicate the period of maximum operculum abduction during the ventilation cycle (measured by video analysis).

 
Efferent stimulation has been shown to reduce the activity of afferent fibers of the lateral line (5). Other studies also illustrated efferent inhibition of the lateral line in response to visual octavolateralis stimuli (6). However, in this study, all fibers were activated by swimming and 40% were activated by ventilatory activity. Thus reafferent noise does not appear to be inhibited by efferent activity at the primary afferent level. Consequently, self-generated noise is possibly filtered from the signal in higher order neurons. Bodznick and Montgomery (7) indicate that the lateral line medullary nuclei contain an adaptive filter capability that cancels inputs consistently associated with an animal’s own movements. Fish are generally mobile animals; however, the ability of the lateral line to function during self movement is largely unknown. This study reports preliminary findings of enhanced nerve activity of the anterior lateral line during self-generated motion, indicating that perhaps mechanosensory noise is not inhibited in afferent activity.

This work was supported by the Minnesota Sea Grant College Program supported by the NOAA Office of Sea Grant, United States Department of Commerce, under grant No. NOAA-NA16-RG1046 (AFM). The U.S. Government is authorized to reproduce and distribute reprints for government purposes, not withstanding any copyright notation that may appear hereon. This paper is journal reprint No. JR-494 of the Minnesota Sea Grant College Program. This work was also supported by Sigma Xi Grants in Aid of Research (LMP).

Literature Cited

  1. Montgomery, J., S. Coombs, and M. Halstead. 1995. Rev. Fish. Biol. Fish. 5: 399–416.
  2. Mensinger, A. F., and M. Deffenbaugh. 1998. Biol. Bull. 195: 194–195.[Web of Science][Medline]
  3. De Rosa, F., and M. L. Fine. 1988. Brain Behav. Evol. 31: 312–317.[Medline]
  4. Russell, I. J., and B. L. Roberts. 1974. J. Comp. Physiol. 94: 7–15.
  5. Flock, A., and I. J. Russell. 1976. J. Physiol. 257: 45–62.
  6. Tricas, T. C., and S. M. Highstein. 1991. J. Comp. Physiol. A. 169: 25–37.[Medline]
  7. Montgomery, J. C., and D. Bodznick. 1994. Neurosci. Lett. 174: 145–148.[Web of Science][Medline]



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 J. Exp. Biol.Home page
L. M. Palmer, M. Deffenbaugh, and A. F. Mensinger
Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus)
J. Exp. Biol., September 15, 2005; 208(18): 3441 - 3450.
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