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First published online November 17, 2006
Journal of Experimental Biology 209, 4788-4801 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02582

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Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus)

Shennan A. Weiss^1,*, Steven J. Zottoli², Samantha C. Do¹, Donald S. Faber¹ and Thomas Preuss¹

¹ Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA and
² Department of Biology, Williams College, Williamstown, MA 01267, USA

View larger version (7K): [in a new window]   Fig. 1. Illustration of the generation and properties of the visual looming stimulus. (A) An LCD projector projects a black disk that grows in size with time on to a translucent white screen. This produces a growing image on the retina, and its size can be quantified as the view angle =2xtan-1 (d/2xs), where d is the diameter of the projected disk on the screen and s is the distance from the screen to the eye. (B) Two looming stimuli 1 and 2, plotted as vs time. Both have the same final view angle, but stimulus 2 grows more slowly than 1.

View larger version (155K): [in a new window]   Fig. 2. Myelinated axons at the level of the recording site, 5 µm transverse section 500 µm posterior to the caudal edge of the facial lobe. The mlf is on either side of the midline. The dorsal portion, mlfd, contains the large M-axon (asterisk) and is separated from the ventral portion, mlfv, by a commissure (arrow). The surface of the hindbrain and the 4th ventricle are dorsal to the M-axons.

View larger version (113K): [in a new window]   Fig. 3. Reticulospinal somata backfilled with dextran biotin from near the chronic recording site. (A) Horizontal section highlighting hindbrain segmentation. Reticulospinal neurons ipsilateral to the injection site are seen in rhombomeres (r-) 4 and 5 and contralateral in r3, r4 and r6 (Bi-Biv). Transverse sections of representative reticulospinal neurons in r2, r4, r5 and r7, respectively. (Bi) Two ipsilateral reticulospinal neurons in r2. (Bii) Bilateral reticulospinal neurons labeled in r4. Note the Mauthner cell ventral dendrite on the left (arrow). (Biii) Bilateral reticulospinal neurons in r5 at the level of the decussation of the M-axons (asterisk). (Biv) Bilateral reticulospinal neurons located in r7. Midline is to the left in Bi and is centered in Bii-Biv.

View larger version (63K): [in a new window]   Fig. 4. Segmental localization and reconstruction of reticulospinal neurons with contralateral axons adjacent to the M-axon in the mlfd. (Ai) Whole mount of the hindbrain, with Lucifer Yellow filled M-axons (upper arrows) and one reticulospinal neuron located in r6 (lower arrow). The M-cell somata are not filled. Higher magnification of the same r6 reticulospinal neuron obtained after sectioning the hindbrain (Aii) and a camera lucida reconstruction of this neuron (Aiii). (Bi,Bii) reconstruction of two other r6 neurons from separate fish. In Aii-Aiii and Bi-Bii, the crossing axons of the reticulospinal neurons are labeled with asterisks, the midline is to the right and scale bars are 50 µm.

View larger version (45K): [in a new window]   Fig. 5. Discrimination of the M-spike with extracellular recordings in caudal hindbrain. (A) Schematic representation of the experimental arrangement, superimposed drawings of the M-cells onto the medulla oblongata with simultaneous paired intra- and extracellular recording were used for B-E. CB, cerebellum; VII, facial lobe; X, vagal lobes (B,Ci,Cii) Extracellular responses recorded close to the left M-axon. Stimulus intensity was gradually increased from subthreshold for both M-axons (black), to above threshold for one (blue) or both (red). Asterisk indicates M-spike(s). (Ci,Cii) Amplitudes of the surface M-spike fields in B as functions or recording distance from the midline of the caudal hindbrain (Ci) and the amplitude of the single spike at the midline as a function of depth from the surface (Cii). Negative depths are in the saline superfusate. (D) Hindbrain field potentials evoked by orthodromic M-cell activation. Suprathreshold current injection in the left M-cell soma (top), and the corresponding M-axon spike and compound action potentials in the hindbrain (middle). After moving the intracellular electrode to the left M-soma (not shown), the directly activated left M-axon spike and compound field potentials was recorded instead (asterisk) (bottom). Asterisk and horizontal broken line indicate M-axon spike and M-triggered activity, respectively. (E) Compound fields correlated with sound evoked M-cell spike activity. The sound stimulus (top) evoked an EPSP recorded from the M-soma before (red) and after (blue) Cl- injection; (bottom) corresponding fields recorded in the hindbrain. Note the two M-spikes (asterisks) are separated temporally by M-triggered activity (broken line).

View larger version (21K): [in a new window]   Fig. 6. Discrimination between left and right M-axon activity. Ai-Aiv and Bi-Biv are from two separate experiments, with the implanted electrode closer to the left or right M-axon, respectively. (Ai,Bi) Superimposed fields obtained when the fish turned to the right (solid trace) or to the left (broken trace). Note that in each case the larger M-spike corresponds to activation of the closer M-axon. (Aii,Bii) Plots of M-spike amplitudes versus trial number. Silhouettes demonstrate corresponding C-start direction. Closed square, open square, and open triangle indicate pip, ramped sound wave or visual looming stimuli, respectively. (Aiii,Aiv,Biii,Biv) Examples of responses associated with C-starts away from the side of the implanted electrode, i.e. to the right and left, respectively. Stimuli were sound pips in Aiii,Biii, a ramped sound wave in Aiv, and a visual looming stimulus in Biv; asterisk indicates M-spike.

View larger version (14K): [in a new window]   Fig. 7. Simultaneous recordings of the hindbrain field potential and the trunk EMG during C-start escape evoked by a pip (A) or a ramped 200 Hz sound wave (B). Asterisks and crosses indicate M-spike and movement onset, respectively. Right panels show evoked fields at an expanded time scale, vertical dotted line indicates estimated time of EMG onset.

View larger version (28K): [in a new window]   Fig. 8. Correlation between longer latency hindbrain field potentials and C-start trajectories with counterturns. (Ai) Representative field potential (red) associated with a C-start to the right superimposed on the mean for all right responses (n=30) ± 1 s.d. waveform. Asterisk indicates M-spike. (Aii) Top: same field potential as in Ai but at a compressed time scale. Insert above: composite plot of the fish's heading at 5 ms intervals. Middle and bottom: fish heading (red) and angular velocity (green) during the corresponding C-start. (Bi,Bii) Same format as for Ai,Aii but in this case, the selected response (red) deviated from the population mean by more than 1 s.d. 12 ms after the M-spike (Bi) and was associated with a counterturn (Bii).

View larger version (10K): [in a new window]   Fig. 9. Comparison of the average RMS field potentials associated with C-starts that do (solid lines) or do not (broken lines) exhibit counterturns. RMS field potentials were aligned at the onset of the individual responses. Error bars are ± 1 s.d. Horizontal arrows indicate the time sequence at which the different stages of the escape behavior take place following the onset of the M-spike (vertical arrow).