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Cover ArticleResearch Articles, Systems/Circuits

Mosaic Organization of Body Pattern Control in the Optic Lobe of Squids

Tsung-Han Liu and Chuan-Chin Chiao
Journal of Neuroscience 25 January 2017, 37 (4) 768-780; DOI: https://doi.org/10.1523/JNEUROSCI.0768-16.2016
Tsung-Han Liu
1Institute of Molecular Medicine,
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Chuan-Chin Chiao
1Institute of Molecular Medicine,
2Institute of Systems Neuroscience, and
3Department of Life Science, National Tsing Hua University, Hsinchu 30013, Taiwan
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  • Figure 1.
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    Figure 1.

    The optic lobe of the oval squid, S. lessoniana. A, Live specimen. Dashed outlines depict a pair of optic lobes located behind the eyes. B, Schematic diagram showing the position of the optic lobe (gray area) relative to the eye in the lateral view of the oval squid. C, Dissected left optic lobe showing the medial view of the optic lobe, where the site of the optic tract can be seen (dented area). A, Anterior; P, posterior; D, dorsal; V, ventral. Scale bars: A, 1 cm; C, 0.5 cm.

  • Figure 2.
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    Figure 2.

    Electrical stimulation in the medulla of the optic lobe is localized. A, Recorded voltage responses decreased significantly as the distance from the stimulation site increased (400, 800, and 1200 μm) for various stimulation voltages used in the present study. B, Stimulating current was significantly reduced at the site 400 μm away from the stimulation site for various stimulation voltages (400 μm, n = 16; 800 μm, n = 16, 1200 μm, n = 4). Error bars indicate SEM.

  • Figure 3.
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    Figure 3.

    Depth of the electrical stimulation site in the optic lobe. Two parasagittal sections of the optic lobe are shown. A, Optic lobe near the medial side showing the optic tract (asterisk). B, Optic lobe near the lateral side. Both sections show clearly the cortex and medulla of the optic lobe. To calculate the relative depth of the stimulation site (red dot), the center of the medulla (yellow dot) was determined either using the inner border of the optic lobe as in A or using the central mass of the optic lobe as in B. Blue line perpendicular to the cortex of the optic lobe indicates the total depth. Relative depth of the stimulation site is thus defined as travel distance of the electrode from the cortex divided by the total depth. Note that the optic lobe in B apparently has two zones of cell islands and this is a result of concave surface of the optic lobe at the lateral side. Scale bar, 1000 μm.

  • Figure 4.
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    Figure 4.

    Body pattern components of the oval squid S. lessoniana. A total of 14 distinct body pattern components were observed in the present study and are shown in these drawings. Except for dark longitudinal stripe and mantle margin stripe, which are shown in a lateral view, all the other 12 components are shown in a dorsal view.

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    Figure 5.

    Subset of body pattern components that are evoked by electrically stimulating the optic lobe of the oval squid. The time series images show the expression of four distinct body pattern components (mantle bands, dark mantle stripe, dark head, and dark arms) after the stimulation onset. Scale bar, 3 cm.

  • Figure 6.
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    Figure 6.

    Stimulation sites in the 3D space of the optic lobe. A, Total of 65 stimulation sites in the present study are shown along three major axes in the optic lobe, including the A–P, M–L, and depth. B–D, Projections of the 3D plot onto 3 2D planes. The dotted outline in B indicates the medulla area of the optic lobe that is accessible to the electrical stimulation. This was estimated by measuring the relative size of the medulla using a series of consecutive histological slices collected from the medial side to the lateral side.

  • Figure 7.
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    Figure 7.

    Stimulation of the optic lobe elicits more ipsilateral expression of chromatophores on the mantle than on the head and arms. The lateralization index is used to assess the symmetry of chromatophore expression upon electrical stimulation in the optic lobe. Positive indices indicate ipsilateral dominance and negative indices show contralateral dominance. Chromatophore expression on the mantle showed significantly ipsilateral control, whereas chromatophore expression on the head and arms was more variable. **p < 0.01.

  • Figure 8.
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    Figure 8.

    Control of chromatophore expression along the body axis has no topographic correspondence in the optic lobe. Stimulation of various optic lobe regions evoked different ipsilateral responses. A, Anterior stimulation (first 1/3 of the optic lobe). B, Middle stimulation (middle 1/3 of the optic lobe). C, Posterior stimulation (last 1/3 of the optic lobe). Regardless the stimulation site, chromatophore expression on the mantle showed the largest increase. Ipsi-mantle, Ipsilateral mantle; Ipsi-head, ipsilateral head; Ipsi-arms, ipsilateral arms. Error bars indicate SEM. *p < 0.05; **p < 0.01.

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    Figure 9.

    Increase in the stimulation voltage enhances ipsilateral chromatophore expression, but not a bilateral response. A, Increase in the stimulation voltage by 2 V (from X to X + 2 V) enlarged the expression area of the chromatophores. B, Increase in the voltage had no significant effect on the bilateral response of chromatophore expression. *p < 0.05.

  • Figure 10.
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    Figure 10.

    Greater depth of stimulation enhances ipsilateral chromatophore expression, but not a bilateral response. A, Greater depth of stimulation by 1 mm (from X to X + 1 mm) enlarges the expression area of the chromatophores. B, Greater depth of stimulation has no significant effect on the bilateral response of chromatophore expression. *p < 0.05.

  • Figure 11.
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    Figure 11.

    Control of the expression of body pattern components is not confined to a specific area of the optic lobe. Each elicited component was scored manually based on the extent of the expression (0 means no expression and 3 means full expression) and the side of the expression (positive means ipsilateral and negative means contralateral). A, Dark head expression was evoked by stimulating widespread locations along the M–L axis in the optic lobe and its activation was more bilaterally dominant. B, Mottled fin expression was elicited by stimulating slightly more restricted areas in the optic lobe and the response was less bilaterally dominant.

  • Figure 12.
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    Figure 12.

    Body pattern components on the mantle are controlled more ipsilaterally within the optic lobe, whereas those on the head and arms are controlled more bilaterally. The lateralization index is used to assess the symmetry of body pattern component expression upon electrical stimulation in the optic lobe. Positive indices indicate ipsilateral dominance, and negative indices show contralateral dominance. Expression of body pattern components on the mantle showed significant ipsilateral control, whereas those on the head and arms showed more bilateral controlled. Numbers in parentheses indicate the sample size. *p < 0.05; **p < 0.01.

  • Figure 13.
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    Figure 13.

    Stimulation sites of the 14 body pattern components in the 3D space of the optic lobe. The stimulation sites of each body pattern component in the present study are shown along the three major axes in the optic lobe, including the A–P, M–L, and depth. Some components were evoked often (e.g., dark mantle), but some were encountered much less often (e.g., fin margin spots).

  • Figure 14.
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    Figure 14.

    Distribution of the evoked probabilities of the 14 body pattern components and their coexpression probabilities with other body pattern components. The central pie chart shows the distribution of evoked probabilities of the 14 body pattern components in the present study. The surrounding pie charts are the distribution of joint probabilities of each body pattern component with other 13 components.

  • Figure 15.
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    Figure 15.

    Electrical stimulation of the optic lobe in anesthetized and quasi-awake animals evokes similar body pattern components. A, Anesthetized animal before stimulation. B, Oval squid showed six distinct body pattern components (DM, DMS, DLS, DH, DA, and DT; see below for abbreviations) during electrical stimulation. C, After 5 min recovery from anesthesia, the animal restored normal ventilation. D, This half-awake oval squid showed identical but stronger body pattern components when the same electrical stimulation was applied again. E, After 6 min of recovery from anesthesia, the animal displayed fin movement. F, Quasi-awake oval squid showing additional two body pattern components (MF and ES) when the same electrical stimulation was applied again. DM, Dark mantle; DMS, dark mantle stripe; DLS, dark longitudinal stripe; DH, dark head; DA, dark arms; DT, dark tentacles; MF, mottled fins; ES, eye spots.

  • Figure 16.
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    Figure 16.

    Coexpression of body pattern components in living oval squid. Various body patterns of oval squids were observed in the wild and in the laboratory. These body patterns are composed of different numbers of components. A, Six body pattern components are shown, but some of them were only weakly expressed. B, Four distinct components are expressed in this oval squid. C, Three components are shown in this male oval squid when attempting to mate with a female. D, Four components are expressed differentially in this squid. The numbers on the top indicate the expression level of individual components.

  • Figure 17.
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    Figure 17.

    Mosaic organization of body pattern control in the optic lobe and the downstream neural processing stages. A, Conceptual diagram based on the findings of the present study illustrating that the control units of individual body pattern components are organized in a mosaic fashion in the motor command module involved in body pattern generation. Each module contains all the control units of body pattern components with different proportions. These modules are spread widely across the medulla of the optic lobe. Therefore, when stimulating any module in the optic lobe, various numbers of different components can be evoked. In turn, different body patterns can be generated by activating distinct subregions in the module. Note the module depicted here represents a continuous structure of cell islands in the medulla. B, Flow chart showing the neural processing stages responsible for body pattern generation. Visual information from eye is integrated by mosaic modules in the optic lobe, then the optic lobe sends motor commands to the downstream lobes such as the peduncle lobe, lateral basal lobe, and chromatophore lobe to control the chromatophore organs.

Tables

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    Table 1.

    Joint probability of coexpression of two body pattern components

    DMMBMFDFMFMSDMSDLS
    DA0.94DM0.63DM0.96DM1.00MB1.00DM0.89DA0.89
    DT0.80DH0.50DA0.88MF1.00DH1.00DA0.86DM0.83
    DMS0.70DA0.50DT0.83MH1.00DM0.00DT0.81DT0.83
    DH0.52DT0.50DMS0.71DA1.00MF0.00DH0.56DMS0.72
    MF0.50MF0.38DH0.50DT0.67DFM0.00MF0.47DH0.50
    DLS0.33DMS0.38SE0.38MB0.33DMS0.00DLS0.36ES0.39
    MH0.28MMS0.25MH0.33MMS0.33DLS0.00MMS0.31MF0.33
    MMS0.26ES0.25ES0.29FMS0.00MMS0.00SE0.28MMS0.28
    ES0.26DFM0.13DLS0.25DMS0.00ES0.00ES0.25MH0.28
    SE0.26FMS0.13MMS0.25DLS0.00MH0.00MH0.22SE0.17
    MB0.11MH0.13MB0.13ES0.00SE0.00MB0.08MB0.00
    DFM0.07SE0.00DFM0.13DH0.00DA0.00DFM0.00DFM0.00
    FMS0.00DLS0.00FMS0.00SE0.00DT0.00FMS0.00FMS0.00
    MMSESDHMHSEDADT
    DM0.86DA1.00DA0.87DM1.00DM1.00DM0.90DA0.93
    DMS0.79DM0.92DT0.87DA1.00DA0.92DT0.83DM0.86
    DA0.79DT0.77DM0.80DT0.69DMS0.83DMS0.65DMS0.67
    DT0.79DMS0.69DMS0.67MF0.62DH0.83DH0.54DH0.61
    DH0.57MF0.54MF0.40DMS0.62DT0.83MF0.44MF0.47
    MF0.43DLS0.54SE0.33DLS0.39MF0.75DLS0.33DLS0.35
    DLS0.36DH0.54DLS0.30MMS0.39MMS0.33ES0.27MMS0.26
    MH0.36SE0.32MMS0.27DFM0.23ES0.33MH0.27ES0.23
    SE0.29MH0.23ES0.23ES0.23DLS0.25MMS0.23SE0.23
    MB0.14MB0.15MB0.13SE0.15MH0.17SE0.23MH0.21
    DFM0.07DFM0.00FMS0.03MB0.08MB0.00MB0.08MB0.09
    FMS0.00FMS0.00DFM0.00FMS0.00DFM0.00DFM0.06DFM0.05
    ES0.00MMS0.00MH0.00DH0.00FMS0.00FMS0.00FMS0.00
    • DM, Dark mantle; MB, mantle bands; MF, mottled fins; DFM, dark fin margin; FMS, fin margin spots; DMS, dark mantle stripe; DLS, dark longitudinal stripe; MMS, mantle margin stripe; ES, eye spots; DH, dark head; MH, mottled head; SE, shaded eyes; DA, dark arms; DT, dark tentacles.

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    Table 2.

    Body pattern components evoked by electrically stimulating the optic lobe of anesthetized and quasi-awake oval squids

    TrialAnesthetized animalQuasi-awake animal
    1DM, DMS, DH, DA, DTDM, DMS, DH, DA, DT
    2DM, DMS, DLS, DH, DA, DTDM, DMS, DLS, DH, DA, DT
    3DLS, DH, DA, DTDLS, DH, DA, DT, DM, DMS
    4DM, MB, MF, DA, DTDM, MB, MF, DA, DT
    5DM, DMS, DH, DA, DTDM, DMS, DH, DA, DT, MF
    6DM, MB, DLS, SE, DA, DTDM, MB, DLS, SE, DA, DT
    7DM, DMS, DLS, DH, DA, DTDM, DMS, DLS, DH, DA, DT, MF, ES
    • DM, dark mantle; MB, mantle bands; MF, mottled fins; DMS, dark mantle stripe; DLS, dark longitudinal stripe; ES, eye spots; DH, dark head; SE, shaded eyes; DA, dark arms; DT, dark tentacles.

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The Journal of Neuroscience: 37 (4)
Journal of Neuroscience
Vol. 37, Issue 4
25 Jan 2017
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Mosaic Organization of Body Pattern Control in the Optic Lobe of Squids
Tsung-Han Liu, Chuan-Chin Chiao
Journal of Neuroscience 25 January 2017, 37 (4) 768-780; DOI: 10.1523/JNEUROSCI.0768-16.2016

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Mosaic Organization of Body Pattern Control in the Optic Lobe of Squids
Tsung-Han Liu, Chuan-Chin Chiao
Journal of Neuroscience 25 January 2017, 37 (4) 768-780; DOI: 10.1523/JNEUROSCI.0768-16.2016
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Keywords

  • chromatophores
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