Distribution of Voltage Gated K“ Channel B Subunits in the Optic Lobe of Adult, Hatchling, and Embryonic Squid, Loligo opalescens Tammy Wang Hopkins Marine Station Stanford University Spring 1997 Professor William F. Gilly ABSTRACT Kyß subunits associate with a subunits and cause changes in both properties (Kyß1) and expression level (Kyß2) of Ky potassium channels. Kyß1 has been noted to Increase channel inactivation rates when co-expressed with Kva. Increases in glycosylation efficiency and surface protein expression of a subunits have been observed in the presence of Kyß2. A partial KVB CDNA clone (Sgß) was isolated from a squid stellate ganglion CDNA library and tentatively identified as a 82-type. In situ hybridization was used to examine Sgß mRNA distribution in adult, hatchling, and embryonic squid. In optic lobes, RNA probe specific for Sgß preferentially labeled cellular layers containing somata of secondary and tertiary visual neurons, bipolar cells, and large amacrine cells. Based on grain density observations, Sgß was present in nearly all medullar cells of post-embryonic squid. In stage 29+ embryos, Sgß grain density was noticeably lower than in adults and hatchlings. Kyß subunits may be expressed in different cells at various levels during development, adding another level of regulation and possibly playing an important role in increasing Ky channel diversity. INTRODUCTION Voltage gated potassium channels are a diverse group of membrane spanning proteins with functions ranging from regulation of action potentials to cardiac pace¬ making (Connor and Stevens, 1971; Byrne, 1980; Rogawaski, 1985; Hille, 1991) to hormone secretion (Dubois and Rouzaire-Dubois, 1993). Such diversity of function is a result of structural flexibility and variety. Channels are composed of associated a and B-subunits. Ky channels are tetrameric proteins, consisting of 4 a-subunits which must be from the same subfamily (Covarrubias et al. 1991; Li et al. 1992; Sheng et al. 1993: Wang et al. 1993; Deal et al. 1994). Some Ky families also associate with cytoplasmic B-subunits thus increasing structural diversity (Pongs, 1995). In the past, most research on Ky channels has focused on the a-subunit. However, examination of the a-subunit alone may present an incomplete picture of true channel function since both a and B-subunits are present in vivo. Kyßs are divided into two classes by their effects on channel function when co-expressed with a-subunits. Kyßs are cytoplasmic proteins which have been found to interact specifically with the NAB domain of KV1 a-subunits, a region which directs the different a-subunits to form heterotetramers (Yu et al. 1996). The interaction of a and ß in the Kvl family does not seem to require the N-terminus of the B-subunit (Nakahira et al. 1996). Although the in vivo function of B-subunits alone is unknown (Yu et al. 1996), the B-family has been found to have significant effects when co-expressed with a¬ subunits. Five B-subunit CDNAs, arising from three related genes, have been isolated from mammalian heart and brain (Rettig et al. 1994, Majumder et al. 1995; Morales et al. 1995, England et al. 1995a; McCormack et al. 1995; Heinemann et al. 1995: England et al. 1995b). Kyß1 and Kyß3 are known to increase inactivation rates of Kyl channels by using a globular domain at the amino terminus similar to the inactivation "ball" found in certain a-subunits (Hoshi et al. 1990; Rettig et al. 1994). Recent experiments with ß3 suggest that B-subunits may act selectively, only associating with some a subunits (Majumder et al. 1995; Morales et al. 1995). Kyß2 subunits, the most abundant of the B-subunit isoforms in the mammalian brain (Rhodes et al. 1995: Rhodes et al. 1996), appear to lack the amino terminus which functions as the mactivation "ball" of B1 and ß3. Instead, 82, which shares -90% sequence homology with B1 and 83 (Rettig et al. 1994), has been found to play a crucial role during K channel biosynthesis by promoting cotranslational N-linked glycosylation of the initial KV1.2 polypeptide, increasing stability of a-B complexes, and augmenting efficiency of a-subunit expression (Shi et al. 1996). This effect is, in part, believed to involve 82 assisting in the proper folding of a-subunit polypeptides mediated through the cotranslational interaction of ß2 with the a-subunit N-terminal cytoplasmic domain. A partial B CDNA clone (Saß) has been isolated from a squid stellate ganglion CDNA library and includes 3' coding and untranslated regions. In this study, we used in situ hybridization techniques to search for Sgß mRNA in the optic lobe of adult. hatchling, and embryonic squid. The optic lobe, a football-shaped structure adjacent to each eye, is the primary region processing visual information from the eye. Divided into three main regions, the two optic lobes are located on either side of the brain. Secondary and tertiary visual cells are present in the optic lobe, along with numerous other types of interneurons. Although the partial Sgß CDNA clone is missing the 5' end required for unambiguous class identification, alignment with known ß sequences has led us to believe that Saß may be a member of the B2 family. Using in situ hybridization, we were able to locate Saß mRNA in various layers of the adult squid optic lobe. We also searched for ß in the different stages of development to obtain a qualitative idea of distribution patterns. MATERIALS AND METHODS Tissue preparation Live adult squid (Loligo opalescens) were collected in Monterey Bay, California. and were held in tanks with circulating sea water at ambient temperatures (13 - 15 °c). Embryos were from egg capsules laid by the captured squid. Egg capsules, once collected, were kept until hatching in 20 gallon circular tanks with constant flow-through seawater at ambient temperatures. Hatchlings (38 days old) used in this experiment were kept in flow-through tanks and raised on a mixed diet (fed both Artemia and copepods) Tissues used for these experiments were dissected and fixed for approximately one hour in an ice-cold 4% paraformaldehyde solution in PBS (130 mM Nacl, 7 mM NazHPOz, 3 mM NaHzPO4, pH 7.0) directly after decapitation. Only the heads of the embryos were used. Hatchlings had their mantles cut open to facilitate perfusion of Polyfreeze. Tissue was then washed for 3 x 5 minutes in PBS before being cryoprotected 2 x 40 minutes in PBS with 20% sucrose. All procedures were done on ice (4 °C). Tissues were blotted dry and coated with Polyfreeze (Polyscience) before being embedded in Polyfreeze in gelatin capsules over dry ice. 8 - 12 micron sections were cut in a cryostat and dried onto silanated slides. Slides were then washed in PBS followed by graded dehydration through ethanol (50%, 70%, 95%, 100%). One slide per set was stained with multiple stain (toluidine blue and basic fuchsin) and air dried for 2 hours before mounting with Permount and xylene. After drying in the hood, slides were either used for in situ hybridization or stored with dessicant at -70 °c. Probe design and construction Antisense probe (- 200 bp) was synthesized from a partial beta CDNA clone in Bluescript KS+ phagemid (pBeta 3'-)after being linearized with Xmal. (Figure 1) Transcription with T7 RNA polymerase was done using a Riboprobe kit (Promega) in a 5 ml reaction volume with 2S labeled UTP (20 uCilml). Sense probe (- 180 bp) was transcribed from the same plasmid with T3 RNA polymerase after linearizing with BstxI. Labeled probes were purified in Nu-Clean spin columns (IBI) and used in hybridization buffer (62.5% deionized formamide, 12.5% dextran sulfate, 375 mM Nacl, 1.25X Denhardts, 12.5 mM Tris pH 8.0, 1.25 mM EDTA) at a final concentration of about 5 x 106 cpm/ml. Hybridization procedure: The hybridization procedure used was described by Liu and Gilly (1995) and adapted from Simmons et al (1989). Slides were incubated in proteinase K, rinsed in triethanolamine, soaked in acetic anhydride, and washed in 2X SSC. Before probe application, mounted tissue was dehydrated in ethanol, allowed to dry, and vacuum desiccated for 2 hours to prevent tissue loss during hybridization. Probe was heated to 65 °C for 10 minutes. Approximately 300 - 400 ul of heated probe was then applied to slides. A slightly-oversized piece of parafilm was placed on the slide, being careful to avoid trapping bubbles. Slides were stored overnight in small, loosely-covered plastic containers which were subsequently placed in a larger tightly sealed humid container at 60 °C. Parafilm coverslips were soaked off and slides washed in 4X SSC (0.15 M. Nacl, 0.015 M sodium citrate). This was followed by treatment with RNase A and washed in sequentially diluted solutions of SSC. 1 mM DTT was included in all SSc washes. Slides were dehydrated in ethanol (50% and 70% EtOH made with SSC and DII) and dried in a hood. Slides were coated with NTB-2 emulsion (Kodak) and stored in light-tight containers for 7 - 10 days at 4 °C before development (4 min in Kodak D¬ 19). After fixation (Kodak Rapid Fixer), slides were washed for -1 hour in running tap water. They were then washed in acetate buffer (0.54% sodium acetate, 0.96% acetic acid) and stained in 0.5% cresyl violet in acetate buffer for 4 minutes before being processed through 50%, 70%, 95%, 100% EtOH and xylene. Finally, slides were mounted with Permount and xylene and dried in the hood. Quantification of signal density Black and white video images were taken of slides. An imaging program (NIH lmage 1.60/ppc) was used to capture frames from Hi-8 video images. Number of grains was counted in randomly selected areas. The number of grains per unit area was calculated by the imaging program. P-values less than 0.01 from t-tests comparing signal densities were considered significant. RESULTS Optic Lobe Structure in Adult Squid General histology corresponds to that reported by Young (1974) (Appendix 1). The outer granule layer (arrowhead; Figure 2) is about 70 microns thick and contains several different types of cells. Secondary visual cells and large amacrine cells are concentrated in the outer half of the outer granule layer and small amacrine cells are localized to the inner half. The two granule layers are separated by the plexiform zone (asterisk; Figure 2) which contains mostly axon bundles, dendrites, and glia. The inner granule layer has small amacrine cells in the outer half and bipolar cells in the inner region. The majority of the optic lobe consists of the medulla which contains an interwoven network of cells, including tertiary visual cells, separated by areas of neuropil. In situ hybridization in adult optic lobe In situ hybridization of sections with Saß antisense probe showed high leyels of signal density in the peripheral region of the outer granule layer (Figure 3a). Labeling with the sense probe did not show labeling above background levels (Figure 3b). Hybridization of sections with Sgß antisense probe showed various signal densities in different cell layers within the same tissue sample. Labeling in the peripheral outer granule layer where secondary visual cells and large amacrine cells predominate was significantly greater than in the interior of the outer granule layer. containing mostly small amacrine cells (Figure 4a). Labeling in the inner part of the Inner granule layer, with bipolar cells, was significantly greater than in the outer region of the inner granule layer, where small amacrine cells are located (Figure 4b). Signal densities in cells of the medulla were greater than those found in the surrounding neuropil. (Figure 4c) The histogram in Figure 5 describes the quantification of signal densities in each cell layer labeled with antisense probe compared to that labeled with sense probe. Grain counts in layers containing secondary and tertiary visual cells and bipolar cells were significantly greater than those seen in small amacrine cell layers. Also, grain counts were significantly greater in cellular regions of the medulla compared to neuropil regions, indicating lack of Saß mRNA in axons, dendrites, and glia. Differential expression of B during development Cross-sections were taken through the horizontal plane of a 38 day old hatchling. Basic structure of the optic lobe was similar to that of the adult. However. the plexiform zone (asterisk; Figure 6) was much smaller and neuropil did not constitute as much of the medulla in comparison to the adult. Rather, cell clumps filled most of the medulla. Amacrine cell layers were proportionately smaller, taking up less than a quarter of each of the granule layers. Late (294) stage embryo (Segawa et al. 1988) heads were also sectioned. Again, basic histology followed adult optic lobe. However, the plexiform zone was even smaller and in some areas, the two granule layers did not appear to be separated (Figure 7). Almost no neuropil was present and we were unable to differentiate between the different cells of the granule layers. Labeling in the peripheral outer granule layer seems to increase with developmental stages (Figure 8). However, it was not possible to compare signals quantitatively between developmental stages because they were carried out as separate experiments. DISCUSSION We constructed our RNA probe from a partial sequence obtained from the CDNA library of the stellate ganglion. Although an RNase protection assay showed that Saß was expressed in the stellate ganglion, we were unable to locate significant amounts of Saß in this tissue by in situ hybridization. Sgß may be present in low abundance in the stellate ganglion. Because we lacked the N-terminus which is the primary determinant of the type of ß subunit, we compared our sequence with those in the literature in an attempt to classity Saß. Aside from the N-terminal, differences between rat Kyß1 and rat Kyß2 are primarily scattered point differences. (Figure 9) However, many of these point differences are conserved when comparing rat and bovine 82. Our partial clone matched the rat and bovine ß2 in 14 sites where rat and bovine 82 were identical but different from rat ß1. The opposite case, where our Sgß matched rat 81 where rat and bovine B2 were the same, only occurred at 5 sites. Thus, it appears to be likely that Saß belongs to the 82 family. Our in situ hybridization results seem to indicate that in adult squid optic lobe. different amounts of Saß mRNA are found in different cells. Sgß mRNA appears to be found in larger amounts in the regions where secondary visual cells and bipolar cells are located. In contrast, low levels of Sgß mRNA are present in the regions surrounding the plexiform zone which contains mostly small amacrine cells, High signal density was found in some of the cells in the medulla, these possibly being the tertiary visual cells. Saß mRNA did not seem to be present in the neuropil and plexiform layers which lack cell bodies The neurons in the optic lobe process visual information from the eye. The primary visual cells in the eye synapse onto the secondary visual cells in the optic lobe where high density signals were seen. Bipolar cells act as interneurons which transmit information from the secondary visual cells to the tertiary visual cells, the primary output neurons from the optic lobe to the brain. In each of these cell types a high density of labeling was found, relative to the control sections, neuropil, and plexiform zones. Based upon our results, Saß appears to play an important and specific function in squid optic lobe cells. Although we cannot determine the role that Sgß plays until we obtain the full sequence and co-express it with a subunits, the presence of B subunits indicated the potential for regulation of potassium channels in certain optic lobe cells. REFERENCES Byrne, J. H. (1980). Quantitative aspects of ionic conductance mechanisms contributing to firing pattern of motor cells mediating inking behavior in Aplysia californica. J. Neurophysiol. 43: 651-668. Connor, J. A., and Stevens, C. F. (1971). Voltage clamp studies of a transient outward current in gastropod neural somata. J. Physiol. 213, 21-30. Covarrubias, M. J., Wei, A., and Salkoff, L. (1991). Shaker, Shal, Shab, and Shaw express independent K current systems. Neuron 7: 763-773 Deal, K. K., Lovinger, D. M., and Tamkun, M. M. (1994). The brain Ky1.1 potassium channel: in vitro and in vivo studies on subunit assembly and posttranslational processing. J. Neurosci. 14: 1666-1676. Dubois, J. M. and Rouzaire-Dubois, B. (1993). Role of potassium channels in mitogenesis. Prog. Biophys. Mol. Biol. 59: 1-21. England, S. K., Uebele, V. N., Kodali, J., Bennett, P. B., and Tamkun, M. M. (1995a). A novel K+ channel B-subunit (hKvß1.3) is produced via alternative mRNA splicing. J. Biol. Chem. 270: 28531-28534. England, S. K., Uebele, V. N., Shear, H., Kodali, J., Bennett, P. B., and Tamkun, M. M. (1995b). Characterization of a voltage-gated K' channel B subunit expressed in human heart. Proc. Natl. Acad. Sci. USA 92: 6309-6313. Heinemann, S. H., Rettig J., Wunder F., and Pongs O. (1995). Molecular and function characterization of rat brain Kyß3 potassium channel subunit. FEBS Lett, 377: 383-389. Hille, B. (1991). lonic Channels of Excitable Membranes (Sunderland, Massachusetts. Sinauer Associates.) Hoshi, T., Zagotta, W. N., and Aldrich, R. W. (1990). Biophysical and Molecular Mechanisms of Shaker Potassium Channel Inactivation. Science 250: 533-538 LI, M., Jan, Y. N., and Jan, L.Y. (1992). Specification of subunit assembly by the hydrophilic amino-terminal domain of the Shaker potassium channel. Science 257: 1225-1230. Liu, 1. I. and Gilly, W. (1995). Tissue Distribution and Subcellular Localization of Na“ Channel mRNA in the Nervous System of the Squid, Loligo opalescens. Receptors and Channels 3: 243-254. Majumder, K., DeBiasi, M., Wang, Z,. and Wible, B. A. (1995). Molecular cloning and functional expression of a novel potassium channel B-subunit from human atrium. FEBS Lett. 361: 13-16. McCormack, K., McCormack, T., Tanouye, M., Rudy, B., and Stuhmer, W. (1995). Alternative slicing of the human Shaker K' channel B1 gene and functional expression of 82 gene product. FEBS Lett. 370: 32-36. Morales, M. J., Castellino, R. C., Crews, A. L., Rasmusson, R. L., and Strauss, H. C (1995). A novel ß subunit Increases Rate of Inactivation of Specific Voltage gated Potassium Channel a subunits. J. Biol. Chem. 270: 6272-6277. Nakahira, K., Shi, G., Rhodes, K. J., and Trimmer, J. S. (1996). Selective Interaction of Voltage-gated K“ Channel B-Subunits with a-Subunits. J. Biol. Chem. 271. 7084-7089. Pongs, O. (1995). Regulation of the activity of voltage-gated potassium channels by B-subunits. Sem. Neurosci. 7: 137-146. Rettig, J., Heinemann, S. H., Wunder F., Lorra, C., Parcej, D. N., Dolly, J. O., and Pongs, O. (1994). Inactivation properties of voltage-gated K channels altered by presence of beta-subunit. Nature 369: 289-94. Rhodes, K. J., Keilbaugh, S. A., Barrezueta, N. X., Lopez, K. L., and Trimmer, J. S. (1995) Association and colocalization of K' channel a- and B-subunit polypeptides in rat brain. J. Neurosci. 15: 5360-5371. Rhodes, K. J., Monaghan, M. M., Barrezueta, N. X., Nawoschik, S., Bekele-Arcuri, Z., Matos, M. F., Nakahira, K., Schechter, L. E., Trimmer, J. S., (1996). Voltage¬ Gated K' Channel B subunits: Expression and Distribution of Kyß1 and Kyß2 in Adult Rat Brain. J. Neurosci. 16: 4846-4860. Rogawaski, M. A. (1985). The A-current: how ubiquitous a feature of excitable cells is it? Trends Neurosci. 8: 214-219. Segawa, S., W. T. Yang, H.-J. Marthy, and Hanlon, R. T. (1988). Illustrated embryonic stages of the eastern Atlantic squid Loligo forbesi. Veliger 30: 230-243. Sheng, M., Liao, V. J., Jan, Y. N., and Jan. L. Y. (1993). Presynaptic A-current based on heteromultimeric K channels detected in vivo. Nature 365; 72-75 Shi, G., Nakahira, K., Hammond, S., Rhodes, K. J., Schechter, L. E., Trimmer, J. S. (1996). B-subunits promote K' channel surface expression through effects earh in biosynthesis. Neuron 16: 843-852. Wang, H., Kunkel, D. D., Martin, T. M., Schwartzkroin, P. A., and Tempel, B. L. (1993). Heteromultimeric K' channels in terminal and juxtaparanodal regions of neurons. Nature 365: 75-79. voung, J.Z. (1974) Philosophical Transactions and Proceedings of the Royal Socjety. London, B Biological Sciences. 267: 263-302. vu, W., Xu, J., and Li, M. (1996). NAB Domain Is for the Subunit Assembly of both a-d and a-B Complexes of Shaker-like Potassium Channels. Neuron 16: 441. 453. FIGURE LEGENDS Figure 1 pBeta3'¬ Plasmid used in probe preparation. To obtain antisense mRNA, primarily in the 3 Untranslated region (UTR), plasmid was cut with Xmal and transcribed with T7 RNA polymerase. For sense mRNA, used in controls, plasmid was cut with BstXl and transcribed with T3. Figure 2 Adult optic lobe Section was stained with cresyl violet which only stains cell bodies. Scale bal equals 150 microns. Outer granule layer (arrowhead) is separated from the inner granule layer by the unstained plexiform zone (asterisk) which lacks cell bodies and contains only axons and dendrites. Medulla is the region containing the islands of cells separated by neuropil. Figure 3 Outer granule layers labeled with both antisense (a) and sense (b) mRNA probes Scale bars equal 50 microns. Plexiform zone is labeled with a P, and outer granule layer periphery is labeled with an O. Signal density is much higher in tissue labeled with antisense mRNA probe than tissue labeled with sense probe. Figure 4 In situ hybridization of adult optic lobe Scale bar equals 30 microns. (a) Outer granule layer of adult Peripheral region is at top of picture. Higher concentrations of signals are present at the periphery, where secondary visual cells are located, compared to the Inner region where small amacrine cells are present. (b) Inner granule layer of adult Unstained portion at top is plexiform region. Periphery of this layer of cells contains small amacrine cells and signal density is low. High grain density is present in the lower portion of the layer where bipolar cells are located. (c) Adult Medulla Regions surrounding the islands of cells are the neuropil, containing axons. dendrites, and glia. Higher levels of mRNA appear to be present in cell bodies than the neuropil. Figure 5 Histogram showing quantification of signal densities in adult granule layers and medulla Saß signal density was found to vary in different adult squid optic lobe cell layers. Sense levels were consistently low in all cell layers. Density levels were low in layers containing small amacrine cells (inner outer granule layer and outer inner granule layer), but high in layers with visual and bipolar cells. (Antisense: Outer outer granule layer: n = 8; mean + of grains/um“ = 0.0388; s.d. = 0.0154. Inner outer granule layer: n = 8; mean F of grains/um“ = 0.0127; s.d. = 0.00243. Outer inner granule layer n = 6; mean + of grains/um“ = 0.00813; s.d. = 0.00332. Inner inner granule layer: n= 6; mean + of grains/um“ = 0.0182; s.d. = 0.00377. Medulla: n = 11; mean tt of grainslum“ = 0.0284; s.d. = 0.00562. Neuropil: n = 11; mean 4 of grains/um? - 0.00845; s.d. = 0.00218. Sense: Outer outer granule layer: n = 4; mean tt of grains/um“ = 0.00975; s.d. = 0.00437. Inner outer granule layer: n = 4; mean 4t of grainslum“ = 0.00674; s.d. = 0.00198. Outer inner granule layer: n = 4; mean tt of grainslum“ = 0.00714; s.d. = 0.00230. Inner inner granule layer: n = 4; mean 4t of grainslum“ = 0.00871; s.d. = 0.00197. Medulla: n = 4; mean + of grains/um? = 0.0114; s.d. = 0.00121. Neuropil: n = 4; mean 4 of grains/um? - 0.00882; s.d. - 0,00277.) Figure 6 Hatchling granule layers Plexiform zone is labeled with an asterisk and medulla is labeled with an arrow. Scale bar equals 30 microns. Section was stained with cresyl violet and labeled with antisense Saß RNA probe. Inner and outer layers are separated by the plexiform zone Figure 7 Stage 29+ embryo granule layers Scale bar equals 30 microns. Outer granule layer is surrounded by a layer of tissue around the optic lobe and is labeled with an asterisk. Labeling appears to be localized to the peripheral outer granule layer. Inner granule layer (arrow) is beneath the plexiform zone. Figure 8 Comparison of (a) adult, (b) hatchling, (c) embryo outer granule layers Scale bars equal 30 microns. Region just outside the outer granule layer is labeled with an O, and P denotes the plexiform zone. Labeling density appears to Increase in the periphery of the outer granule layer through development. Figure 9 Beta Sequence Alignment of Saß with rat ß1 and 82 and bovine B2 provide evidence that Saß belong to the B2 family. Dashes represent the same residue as in the first line (rat KVB1). Residues are boxed where Saß is the same as rat and bovine 82 but different from rat B1. The underlined region was the 5' end of our probe which continued into the untranslated region. Appendix 1 Young's schematic This schematic represents the optic lobe of an adult squid. The top most layer is the outer granule layer, containing large and small amacrine cells, and secondary visual cells. This is separated from the inner granule layer by the plexiform zone which consists mostly of axons and dendrites. Bipolar cells and small amacrine cells are found in the inner granule layer. The majority of the optic lobe consists of the medulla which contains tertiary visual cells and other cell bodies. Figure 1 T3A &am — Xmal BstXI 180 bp - 200 bp pBeta3'- Bluescript KS+ 3'UTR Beta coding region 2T7 Figure 2 Figure 5 Beta Signal Density Varies in Different Adult Squid Optic Lobe Cell Layers 0.04 - 0.03 00 0 + OOGL IOGI OIGL iIGL Med. Cells Neuropil Cell laye OOGL = outer outer granule layer IÖGL = inner outer granule layer OIGL = outer inner granule layer IIGL = inner inner granule layer Med. Cells = cells in the medulla HAntisense Sense Figure 6 Figure 7 Figure 9 rat Kv BI AMYWGTSRWSAMEIMEAYSVAROF rat Kv 32 - — — — — - - S. — — — — bov Kv ß2-------- - - S- - - - - - - - - - - - - sq Kv ß2 CXG - - - - - - PR - - - - CCA - - - - - rat Kv Bl NMIPPVCEQAEYHLFOREKVEVOL rat Kv 82 ------ -- - -- ---- bov Kv 82 - | | — - - | - - - --- | | - - - - - -- s Kv 2 - - - - --- - NMH -D---LHM rat Kv B1 PELYHKIGVGAMTWSPLACGIISG rat Kv ß2 - - - F - - - - - - - - - - - = = = = = = = V - bov Kv ß2 - - - F - - - - - - - = = = = = = — — — = = V - sq Kv B2 9D I - 9 - - - - - T T - - - - - S - - LT - rat Kv BI KYGNGVPESSRASLKCYQWLKERI rat Kv 82 - -Ds- I-P------G- D KI¬ bov Ky 82 - - D | S - 1 - P y - - - - - -G ---DK. sq Kv 82 - 00 ---v ---A--N-g---pK rat Kv Bl VSEEGRKOONKLKDLSPIAERLGC rat Kv 82 L - - ---R --A---E- 9A---- - - - bov Kv 82 | | - - - - - R - | | - - -E-Al- -- - -- - sq Kv 82 L--D -- --- REVAVVAIDE --- rat Kv BI TLPOLAVAWCLRNEGVSSVLLGSS rat Kv 82 - - - - - | 1 | - - - - - — A- bov Kv ß2 - - - - - - | - - - - - - — — — — — — — — -A sq Kv ß2 s-A-- -I ----- - -T-HC -- - a rat Kv BI TPEOLIENLGAIQVLPKMTSHVVN rat Kv B2 NA- --M--I- -------(s-SI-H bov Kv 82 SAID - M - - | 1 | - - ----LS-SIIH sq Kv 82 slv p-- v --10---Yv---PTLM. rat Kv BI EIDNILRNKPYSKKDRS rat Ky 82 --- § --G- - - - - - - - - bov Kv B2 - - - S - - Gl--- - - - - - - - sq Kv B2 - L-KL-G---L-R--HPPRVFNNP.. 2.tr. opt. Appendix A n.ret.1 n.ret.2 n.ret.3 ceam lar. e.vis 2out. out. gaa. 4 T plex. 8 —œamin. grin. S f ax.ter. palis- ce.vis.2. ce palis 2.fro. 22 32 z.ra. ce mult.lar. ce mult lar. ce multam —ce.vis 3 5 ce mult lar. -n.f.cent. ce.vis.3 z.tan. ax.ter. cecent. 2 3 55 g nfcent. ce vis.3 ceen S Olmm n.f.cent. ce.mult. lar. from J. Z. Young, Central Nervou