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ARTICLE

Sensory Processing in the Pallium of a Mormyrid Fish

James C. Prechtl, Gerhard von der Emde, Jakob Wolfart, Saçit Karamürsel, George N. Akoev, Yuri N. Andrianov and Theodore H. Bullock
Journal of Neuroscience 15 September 1998, 18 (18) 7381-7393; https://doi.org/10.1523/JNEUROSCI.18-18-07381.1998
James C. Prechtl
1Neurobiology Unit, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093,
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Gerhard von der Emde
2Zoologisches Institut, Universität Bonn, 53115 Bonn, Germany,
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Jakob Wolfart
1Neurobiology Unit, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093,
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Saçit Karamürsel
3Center for Electroneurophysiology, Istanbul University School of Medicine, 34390 Istanbul, Turkey, and
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George N. Akoev
4Pavlov Institute of Physiology, Russian Academy of Sciences, 199034 St. Petersburg, Russia
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Yuri N. Andrianov
4Pavlov Institute of Physiology, Russian Academy of Sciences, 199034 St. Petersburg, Russia
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Theodore H. Bullock
1Neurobiology Unit, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093,
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  • Fig. 1.
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    Fig. 1.

    Diagrams of gross anatomy of theGnathonemus brain and the area sampled.A, Cross-hatched area indicates the segment of valvula that was removed on one side for most experiments. Dark shading approximates the area in which most recordings were made. B, Dorsal view of the cerebrum, as though transparent, that summarizes the horizontal distribution of unimodal octavolateral sensory responses. Center of mechanosensory response zone (thick line) lies ∼400 μm ventral to the center of electrosensory area, which is ∼300 μm deep to the dorsal surface with almost no overlap (dashed line). Auditory zone, also 0–500 μm deep, overlaps the electric. Stars represent the diffuse distribution of visually responsive loci, 600–1700 μm below the surface. Cross-section markers a-f indicate transverse reference planes used in Figures 2 and 3. Dd, Telencephalic area dorsalis pars dorsalis; Dm, telencephalic area dorsalis pars medialis; hyp, hypothalamus;LC, caudal lobe; lfb, lateral forebrain bundle; LP, posterior lateral line lobe;TH, thalamus.

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    Fig. 2.

    Forebrain transverse sections corresponding to planes a-f in Figure 1B, used as templates for the reconstruction of sensory-evoked response loci in Figure 3 (30 μm sections; cresyl violet; nomenclature adapted fromNieuwenhuys, 1963). ca, Anterior commissure;Dcd, Dd-associated part of the Dc; Dcm, Dm-associated part of the Dc; Dd, telencephalic area dorsalis pars dorsalis; Dla, telencephalic area dorsalis pars lateralis, part a; Dlb, telencephalic area dorsalis pars lateralis, part b; Dlc, telencephalic area dorsalis pars lateralis, part c; Dlm, telencephalic area dorsalis pars lateralis, medialis; ent, nucleus entopeduncularis;lfb, lateral forebrain bundle; V, telencephalic area ventralis; Vd, telencephalic area ventralis pars dorsalis; Vm, telencephalic area ventralis pars medialis; Vv, telencephalic area ventralis pars ventralis.

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    Fig. 3.

    a-f, Reconstructed distribution of sensory-evoked responses, superimposing data from 18 animals, projected onto six transverse planes (half sections). Sections a-fcorrespond to the planes of the section in Figures1B and 2. Sampled depths in each penetration were usually 50 μm apart; here a small fraction of the loci recorded from are plotted. Responses to each stimulus type are color-coded, and multimodal responses are represented by larger polygons with combinations of color codes. White marks indicate a lack of response to any stimulus; their scatter among responsive loci reflects the between-animal variability in the size and location of unimodal response zones. g, Plan view of left cerebral hemisphere, as in Figure 1B, shows the superimposed unimodal response distributions from four specimens represented by four symbols (triangle,diamond, circle, and star) but with the same color code as in transverse sections. Depth of response sites is not indicated.

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    Fig. 4.

    Aspects of auditory-evoked response recorded in the Dm. A, Depth profile of simultaneous single sweeps of AEP recorded with a multichannel, in-line silicon probe (see Materials and Methods). Vertical lines mark the onset of the 100 msec tone pip. Arrows indicate 35–45 Hz waves that are separated by higher frequency waves and spikes.B, Averaged AEPs to 10 and 300 msec tone pips (thick and thin traces) recorded 100–200 μm below the surface. Traces plotted on log–log scales to emphasize early, small, far-field potentials. The baseline is arbitrarily set at 7–8 μV negative instead of the zero of the AC amplifier. The early positive wave at 4 msec (i.e., P4) has a base-to-peak amplitude of ∼5 μV, whereas the N40 represents a negative excursion of ∼85 μV. Plot is clipped at the beginning of a slow positive potential that lasts for hundreds of milliseconds. Note that the averaging has greatly reduced the high-frequency-induced waves and spikes.

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    Fig. 5.

    Latencies and frequency compositions of sensory-evoked potentials. A, AEP depth profile illustrating a shift of principal wave (N45) to a shorter latency (N30) below 500 μm, which is still an active depth, judging by local spikes. Large arrows indicate the peaks of principal waves. An intermediate form at 500 μm shows a loss of the N45 (small arrow) and emergence of the N30 (star). B, Amplitude spectra show the distribution of power in the different frequency bands before the stimulus and during the response. Shaded areas indicate the mean ± SEM. White areas between the shaded traces are proportional to the reliability of the power increases. Plots based on the averages of averaged responses, 10 auditory, 8 electrical, 6 mechanical, and 4 visual from different animals.

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    Fig. 6.

    Auditory frequency after response. Presentation of repetitive stimuli at different rates (1–5 Hz) shows that the amplitudes of AEPs are markedly attenuated and become labile at rates >2 Hz. Even at 1 Hz, the third and later AEPs are reduced in initial negativity.

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    Fig. 7.

    Responses to electrical and mechanical stimuli at different depths in the pallium. Responses to electrical are superficial, in the caudal half of the Dm. Responses to mechanical stimuli are obtained in a similar area but always more ventrally, beginning ∼700 μm below the surface. Note that in this sample an electrosensory response resumes in an altered form at 800–900 μm. Single sweeps, vertical line marks stimulus onset.

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    Fig. 8.

    Example of a rare multimodal locus, recorded at successive depths at which responses were observed to each of the four stimuli tested (A–D). Single sweeps all from the same animal and locus. The mechanosensory response at this locus includes a late, positive slow wave (P180). The responses to all four stimuli include long-lasting increases in multiunit activity. Note the tendency of visual and mechanical stimuli to induce bursts of corollary discharges (some marked by stars).

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    Fig. 9.

    Samples of stimulus-induced (top trace) and spontaneous (bottom traces) δF waves from three animals. These large waves that begin with relatively slow negative excursions (peaking at 350 msec from the arbitrary time of the sweep start) precede bursts of EODCs and their corollary discharges (some marked by stars). The δF wave of thetop trace occurred after an electrical stimulus whose artifact appears as a vertical line.

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    Fig. 10.

    Stimulus-induced changes in coherence between recording loci. A, In comparison with the immediately prestimulus baseline, coherence during the peak of the response (200 msec window) between neighboring electrodes (200 μm) decreases in the ∼35–50 Hz band and increases in no band <60 Hz. B, Filtered (15–55 Hz) and superimposed traces from three electrodes show the synchrony across the three loci in the ongoing LFP (thin arrows) and the phase shifts that occur during most of the response (thick arrows). C, Reproducible coherence increases in a single animal in the 52–60 Hz band after a visual stimulus. D, Superimposed traces from channels 1 and 3 in panel C before and after filtering.Arrows indicate synchronous high-frequency waves inTrial 1 and dotted lines show the jitter of these waves between trials. A, C,stars represent statistical significance at the 0.05 level, two-tailed t test.)

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    Table 1.

    Average evoked potentials, means of four measures

    Auditory (n = 115)Electrical (n = 34)Mechanical (n = 41)Visual (n = 18)
    Response onset (msec)19  ± 338  ± 236  ± 446  ± 4
    Peak latency (msec)58  ± 368  ± 384  ± 10136  ± 9
    Duration (msec)544  ± 17452  ± 16504  ± 17385  ± 27
    Amplitude (μV)135  ± 1086  ± 1093  ± 10126  ± 11
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The Journal of Neuroscience: 18 (18)
Journal of Neuroscience
Vol. 18, Issue 18
15 Sep 1998
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Sensory Processing in the Pallium of a Mormyrid Fish
James C. Prechtl, Gerhard von der Emde, Jakob Wolfart, Saçit Karamürsel, George N. Akoev, Yuri N. Andrianov, Theodore H. Bullock
Journal of Neuroscience 15 September 1998, 18 (18) 7381-7393; DOI: 10.1523/JNEUROSCI.18-18-07381.1998

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Sensory Processing in the Pallium of a Mormyrid Fish
James C. Prechtl, Gerhard von der Emde, Jakob Wolfart, Saçit Karamürsel, George N. Akoev, Yuri N. Andrianov, Theodore H. Bullock
Journal of Neuroscience 15 September 1998, 18 (18) 7381-7393; DOI: 10.1523/JNEUROSCI.18-18-07381.1998
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Keywords

  • cerebral cortex
  • corollary discharge
  • induced rhythms
  • evoked potential
  • gamma band
  • lateral line
  • mormyrid

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