stored together in nerve terminal vesi-cles of sympathetic nerves (8).

2) Norepinephrine and ATP, whenadded exogenously to the vas deferens,produce contractions that are specifical-ly antagonized by al- and P2-receptorantagonists, respectively.

3) Stimulation of the motor nervesproduces a biphasic contraction, andphases I and II are preferentially antago-nized by the same a1- and P2-receptorantagonists.

4) Reserpine treatment does not abol-ish EJP's in the guinea pig vas deferens(9).

5) Adrenergic antagonists such asphentolamine, phenoxybenzamine, andprazosin readily antagonize phase II butare relatively ineffective in reducingEJP's at similar doses (10).

6) The P2-receptor antagonist AN-APP3 can preferentially block phase I ofthe contraction and the EJP's.

7) Since EJP's are enhanced by prazo-sin and blocked by ANAPP3, it wouldseem unlikely that the two transmitterscould interact in this fashion,if they werereleased from different nerve popula-tions. Furthermore, agents that selec-tively damage sympathetic nerves (suchas 6-hydroxydopamine) can inhibit bothphase I and phase II of the contractileresponse (4), indicating that both depend

There is behavioral evidence that or-

ganisms as diverse as bacteria (1, 2),homing pigeons (3-5), and honey bees (6,7) are sensitive to earth strength magnet-ic fields. In magnetotactic bacteria theresponse to magnetic fields is based on

intracytoplasmic magnetite (Fe3O4) par-

ticles that impart a permanent magneticdipole moment to these prokaryotes (1,2). The sensory systems that detect mag-netic fields in homing pigeons and honeybees are still unknown. However, re-

ports of magnetite in both homing pi-geons (8) and honey bees (9) as well as inother organisms (10, 11) suggest that thisiron oxide could also be the basis ofmagnetic field detection in eukaryotes.Since magnetite in honey bees is report-ed to be localized in the abdomen (9), wehave histologically examined tissues ofthe honey bee abdomen and looked spe-

cifically for those cells that contain ironand for connections between these cellsSCIENCE, VOL. 218, 12 NOVEMBER 1982

on release of transmitter from adrenergicneurons.

8) Finally, ATP and norepinephrineare synergistic in producing contractionwhen added exogenously, and exoge-nous ATP enhances contractile respons-es to nerve stimulation (11).

P. SNEDDON*D. P. WESTFALL*

J. S. FEDANDepartment of Pharmacology andToxicology, West Virginia UniversityMedical Center, Morgantown 26506

References and Notes

1. N. Ambache and Zar M. Aboo, J. Physiol.(London) 216, 359 (1971).

2. J. C. McGrath, ibid. 283, 23 (1978).3. G. K. Hogaboom, J. P. O'Donnell, J. S. Fedan,

Science 208, 1273 (1980).4. J. S. Fedan, G. K. Hogaboom, J. P. O'Donnell,

J. E. Colby, D. P. Westfall, Eur. J. Pharmacol.69, 41 (1981).

5. A. G. H. Blakeley, D. A. Brown, T. C. Cun-nane, A. M. French, J. C. McGrath, N. C.Scott, Nature (London) 294, 759 (1981).

6. G. D. S. Hirst and T. C. Neild, ibid. 283, 767(1980).

7. P: Sneddon, D. P. Westfall, J. Colby, J. S.Fedan, Fed. Proc. Fed. Am. Soc. Exp. Biol. 41,1720 (1982).

8. K. B. Helle, H. Langercrantz, L. Stjarne, ActaPhysiol. Scand. 81, 565 (1971).

9. G. Burnstock, M. E. Hollman, H. Kuriyama, J.Physiol. (London) 172, 31 (1964).

10. G. Burnstock and M. E. Hollman, Br. J. Phar-macol. 23, 600 (1964).

11. T. Kazic and D. Milosavljevic, ibid. 71, 93(1980).

* Present address: Department of Pharmacology,University of Nevada School of Medicine, Reno89557-0046.

20 July 1982; revised 25 August 1982

and the central nervous system, a re-

quirement for a sensory receptor.We have found bands of cells in each

abdominal segment of the honey bee thatcontain numerous iron-rich granules. Wehave localized the cells and the granulesby both light and electron microscopy.

For light microscopy we stained withPrussian blue, a reaction in which ironforms a blue precipitate in the presenceof acidic potassium ferrocyanide. Forelectron microscopy we relied on elec-tron opaqueness coupled with x-ray mi-croanalysis to identify the iron granules.Using Mossbauer spectroscopy we iden-tified the iron granules as consisting prin-cipally of hydrous iron oxides.For gross examination of the honey

bee abdomen (Fig. 1), adult foragingworkers were pinned on dental wax, andtheir abdomens were cut and pinnedopen with stainless steel minutien pins.The abdominal contents were fixed andstained in situ (12). The dissected abdo-mens were then washed in distilled waterand examined with a Zeiss dissectingmicroscope. The stained cells (Fig. 1)occur in a band under the epidermis ineach abdominal segment. There is ahigher concentration of cells in the ven-tral abdomen under each segmental gan-glion. Sheets of this tissue were re-moved; examination revealed that theiron-positive staining cells form a reticu-lar network within which is another pop-ulation of smaller spherical nonstainingcells. In fresh, unstained tissue these twocell types are easily distinguished, andthe iron-containing cells are seen to havegranules of a yellowish color.

Examination of dissected whole abdo-mens stained with methylene blue showsthat at each segmental ganglion a smallnerve branch enters into the iron-posi-tive tissue layer and ramifies throughoutit. Mechanical movement of this smallnerve trunk causes movement of thistissue layer but no other observablestructures. Thus, it seems that this tissueis supplied with an efferent or afferentnerve supply (or both).For light microscopy tissue was fixed

and embedded in plastic. Sections (3 p.mthick) wer_ mounted on slides andstained for iron with the acidic potassiumferricyanide. The sectioned material(Fig. 2) shows the two cell types that

Fig. I (left). Honey bee abdomen pinned open and stained for iron. Arrows show large groups ofiron-staining (dark) cells under segmental ganglion. Fig. 2 (right). Light photomicrograph ofa section of the ventral portion of an abdominal segment containing oenocytes and fat cells(arrows). The oenocytes are characterized by a granular staining pattern; c, cuticle.

0036-8075/82/ 1112-0695$01 .00/0 Copyright 1982 AAAS

Iron-Containing Cells in the Honey Bee (Apis mellifera)Abstract. Honey bees are sensitive to earth strength magnetic fields and are

reported to contain magnetite (Fe304) in their abdomens. We report bands of cellsaround each abdominal segment that contain numerous electron-opaque, iron-containing granules. The iron is principally in the form of hydrous iron oxides.

695

on Septem

ber 10, 2020

http://science.sciencemag.org/

Dow

nloaded from

Fig. 3. (a) Low magnification transmission electron micrograph of iron-containing cell andneighboring fat cell (F). Dark granules are perinuclear iron containing granules. Many vesiclescan also be seen (x 1,320). (b) High-magnification transmission electron micrograph showingan area containing iron granules, vesicles (V), and rough endoplasmic reticulum (arrows); scalebar, = 0.5 ,um (x 19,200).

were observed in the whole mounts. Thesmaller cells never show any sign of a

positive staining for iron. while the largercells always show a granular stainingpattern.We also examined this tissue in the

transmission electron microscope. Ex-cised tissue was fixed and embeddedconventionally. Silver sections were cutwith a diamond knife and stained withuranyl acetate and lead citrate. Ultra-structurally one can distinguish the twocell types. The smaller, spherical cellshave an abundant endoplasmic reticulumand contain many vesicles. These appearto be the fat cells described by Snodgrass(13). The other cells (Fig. 3a) are larger,more irregular in shape, and also haveextensive rough endoplasmic reticulumfree ribosomes, and many vesicles.These cells also contain many small (0.1to 0.9 ,um) round, very electron opaqueparticles. At high magnification (Fig. 3b)these particles do not seem to be mem-brane bound, and they do not have anyobvious substructure.The electron opaque particles in thick

(1500 to 2000 A) sections of unosmicatedtissue embedded in Epon 812 were stud-ied by electron diffraction and energy-dispersive x-ray microanalysis. Theseanalyses were done on a JEOL 200CXoperating at 200-kV accelerating voltage.The x-ray analytical system utilizes an

energy dispersive Si(Li) detector. Select-ed area diffraction patterns showed onlythe weak diffuse rings from the Epon. Noevidence of crystalline material was ob-served in either the selected area or

microdiffraction modes. On the basis ofthe size of the particles, the sectionthickness, and the quantity of iron in theparticles as suggested by the x-ray analy-

696

sis (see below), a diffraction patternwould be expected if significant crystal-line structure existed.X-ray spectra were obtained in the

STEM mode with a 200-A spot countingfor 200 seconds with the use of a lowbackground graphite specimen holderwith a specimen tilt of 400. The spectrafrom an electron opaque granule (Fig.4a) show a large quantity of iron presentas compared to an immediately adjacentarea devoid of granules (Fig. 4b). Spec-tra taken in the CTEM mode with a 0.1-p.m spot gave the same results. Theseparticles also contain calcium and phos-phorus as seen in Fig. 4a.To characterize the chemical state of

Fig. 4. (a) Energy dispersive x-ray spectrumof electron dense granules. STEM mode witha spot size of 200 A at 200-kV acceleratingvoltage was used. Counts were for 200 sec-onds with a background of 20 to 40 counts. (b)Energy dispersive x-ray spectra of adjacentcell area devoid of granules; same conditionsas (a).

the iron in the granules, 57Fe Mossbauerspectroscopic measurements at 4.2, 160,and 300 K were made on bands of iron-rich cells that had been excised fromhoney bees and placed in distilled waterand lyophilized. The Mossbauer spec-trum (data not shown) of 180 mg oflyophilized cells pooled from 300 beesconsists of a broadened quadrupole dou-blet at 160 and 300 K, based on a com-puterized, least squares fit to the data;the quadrupole splitting and isomer shiftat 160 K are 0.65 mm/sec and 0.46 mm/sec (relative to iron metal at 300 K),respectively. At 4.2 K the spectrumshows evidence of nonhomogenous mag-netic hyperfine splitting. These spectralcharacteristics indicate densely packedferric iron with oxygen coordination sim-ilar to iron in biological iron storagematerials including ferritin and othersthat contain amorphous iron oxides (14).In particular, hydrous iron oxide gran-ules associated with calcium and phos-phorus are known in the marine inverte-brate Molpadia intermedia (15).The iron-rich granules occupy approx-

imately 7 percent of the 3 x 10-8 cm3volume of the cells which contain them.Passage of trypsinized cells through aCoulter counter which selected for thelarge cells gives approximately 11,300 ofthese cells per bee. Thus the estimatedvolume of the granules is 2.5 x 10-5 mlper bee or 7.2 x l0-5 g, if the density is3.0. Gould et al. (9) measured an averageinduced magnetic moment of about2 x 10-6 E.M.U. per bee correspondingto at least 2.2 x 10-8 g of Fe3O4. Sincehydrous iron oxides are typically para-magnetic at room temperature (16, 17)they would not contribute to the rema-nent magnetism of the bee. However,only 0.33 percent of the hydrous ironoxide present would have to be reducedto magnetite to account for the measuredmagnetic moment. Hydrous iron oxidesare precursors to Fe3O4 formation inchitons and magnetotactic bacteria (2,18). This small quantity of Fe3O4 wouldnot be detected with any of our analyti-cal techniques.We believe that these iron-containing

cells are the oenocytes of the honey beeas described by Snodgrass (13). Thesecells have been studied in the larvae ofother insects [Gryllus bimacultaus (19)and Calpodes ethilius (20)] where theyseem to be involved in steroid synthesisduring development. Their function inthe adult is at present unknown. Thereare no reports, however, that these cellscontain either dense granules or iron inany insect except in our studies of adultbees.

SCIENCE, VOL. 218

on Septem

ber 10, 2020

http://science.sciencemag.org/

Dow

nloaded from

In summary, the oenocytes of theadult foraging honey bee form an inner-vated sheet of tissue around each ab-dominal segment. Each cell of the sheetcontains many electron-opaque iron-con-taining granules in the cytoplasm.

DEBORAH A. KUTERBACHBENJAMIN WALCOTT

Department ofAnatomical Sciences,Health Sciences Center, StateUniversity ofNew York at Stony Brook,Stony Brook, Long Island 11794

RICHARD J. REEDERDepartment of Earth and SpaceSciences, State University of New Yorkat Stony Brook

RICHARD B. FRANKELFrancis Bitter National MagnetLaboratory, Massachusetts Institute ofTechnology, Cambridge 02139

References and Notes1. R. Blakemore, Science 190, 377 (1975).2. R. B. Frankel, R. P. Blakemore, R. S. Wolfe,

ibid. 203, 1355 (1979).3. W. T. Keeton, Proc. Natl. Acad. Sci. U.S.A.

68, 102 (1971).4. _, T. S. Larkin, D. M. Windsor, J. Comp.

Physiol. 95, 95 (1974).5. C. Walcott and R. P. Green, Science 184, 180

(1974).

recognition of details of the movement.

Practice can improve ability to dis-criminate among objects. This perceptu-al learning often simply reflects im-proved ability to pick out features distin-guishing one visual target from another(1, 2). Other times, perceptual learningrequires a change in the observer's useof verbal labels to describe his experi-ence (3) or heightened attention or arous-al (4). We report an enduring alterationin vision that is specific to the stimuluson which an observer is trained. Ratherthan resulting from an increased abilityto pick out some critical feature of thestimulus, this form of perceptual learn-ing may be related to changes in theselectivity of elements in the visualsystem.

Since previous work suggested thatmotion perception is plastic (5, 6), we setout to train an observer's discriminationof the direction of moving targets. Be-fore training, we measured how wellobservers discriminated small differ-

SCIENCE, VOL. 218, 12 NOVEMBER 1982

6. M. Lindauer and H. Martin, Z. Vgl. Physiol. 60,219 (1968).

7. H. Martin and M. Lindauer, J. Comp. Physiol.82, 145 (1972).

8. C. Walcott, J. L. Gould, J. L. Kirschvink,Science 205, 1027 (1979).

9. J. L. Gould, J. L. Kirschvink, K. S. Deffeyes,ibid. 201, 1026 (1978).

10. J. Zoeger, J. R. Dunn, M. Fuller, ibid. 213, 892(1981).

11. T. P. Quinn, R. I. Merrill, E. L. Brannon, J.Exp. Zool. 217, 137 (1981).

12. Fixation was with either 4 percent Formalin or2.5 percent glutaraldehyde in phosphate buffer.Staining was with a hot (60'C) 1:1 mixture of 0.5percent potassium ferricyanide and 0.5 percentHCI for 15 to 30 minutes.

13. R. E. Snodgrass, Anatomy of the Honey Bee(Comstock Publishing Association, Cornell Uni-versity, Ithaca, N.Y., 1956).

14. S. Ofer, G. C. Papaefthymiou, R. B. Frankel, H.A. Lowenstam, Biochim. Biophys. Acta 679,199 (1981).

15. H. A. Lowenstam and G. R. Rossman, Chem.Geol. 15, 5-5 (1975).

16. A. Blaise, J. Chappert, J. L. Giravdet, C.R.Acad. Sci. Paris 261, 2310 (1965).

17. J. M. D. Coey and P. W. Readman, EarthPlanet. Sci. Lett. 21, 45 (1973).

18. K. M. Towe and H. A. Lowenstam, J. Ultra-struct. Res. 17, 1 (1967).

19. F. Romer, Cell Tissue Res. 151, 27 (1974).20. M. Locke, Tissue Cell 1, 103 (1969).21. B.W. is supported by grant GM 28804 from the

National Institutes of Health. R.B.F. is partiallysupported by the Office of Naval Research. TheFrancis Bitter National Magnet Laboratory issupported by the National Science Foundation.We thank C. McKeon for help with tissue isola-tion and G. C. Papaefthymiou for help with theMossbauer data analysis.

I April 1982; revised 15 June 1982

ences in direction of motion. Discrimina-tion was assessed around eight differentdirections: 0° (rightward), 450, 900 (up-ward), 135°, 1800, 225°, 2700, and 315°.Hereafter, we refer to directions 00, 900,1800, and 2700 as principal directions and450, 1350, 2250, and 3150 as oblique direc-tions. Eight observers were tested: onewas K.B. and six were naive about ourpurposes.

Stimuli were bright, spatially randomdots moving along parallel paths over theface of a cathode ray tube at 10° persecond. At any one time, about 400 dotswere visible within an 80 circular aper-ture. The dots, and their movement,were highly visible: the luminance of thedots was approximately 50 times thatrequired for them to be just seen againsta constant veiling luminance of 2 cd/m2.Opposite ends of the display were linkedelectronically so that dots disappearingat one side wrapped around, to reappearat the opposite side. Full details of the

display are given elsewhere (6). Observ-ers viewed the displays binocularly, fix-ating a dark, stationary, central point. Toguard against the possibility that observ-ers might learn to identify details of ourdisplay, a new array of spatially randonmdots was used every 50 trials (7).Each trial consisted of two 500-msec

intervals. This pair of intervals was sepa-rated by a 200-msec period during whichonly the uniformly illuminated cathode-ray tube was visible. Two equiprobabletypes of trials, "same" and "different,"were randomly ordered. On "same" tri-als, motion took the same direction dur-ing both intervals; on "different" trials,motion in one interval was in a directiondiffering by 30 from that of the otherinterval. The observer viewed both inter-vals and judged the two directions"same" or "different."A block of 50 trials was characterized

by one standard direction. This directionappeared in both intervals of "same"trials and in one interval of "different"trials. In the remaining interval of "dif-ferent" trials, a random choice wasmade to present motion 30 either clock-wise or counterclockwise of the standarddirection. Whether the first or secondinterval contained the standard directionon "different" trials was also randomlydetermined. A tone after each correctjudgment gave immediate knowledge ofresults.The main experiment required seven

sessions over 10 to 12 days. In sessions1, 4, and 7, discrimination performancewas measured for all eight directions.The order of testing was separately ran-domized for each session and observer.In sessions 2, 3, 5, and 6, an observertrained on just one of the eight direc-tions, principal and oblique. At the startof the experiment, a different trainingdirection was assigned each observer,who retained that assignment throughoutthe experiment. During a training ses-sion, an observer made 500 "same-dif-ferent" judgments (ten blocks of 50 tri-als) with the assigned direction. For bothtraining and test sessions, observerswere rewarded with 2 cents for eachcorrect response; 1 cent was deductedfor each incorrect response.Responses in a block of trials were

reduced to a pair of proportions: theproportion of "different" trials correctlyidentified as such (hits), and the propor-tion of "same" trials misidentified as"different" (false alarms). These propor-tions were converted into d', a measureof discrimination performance (8). Thismeasure granted immunity to spuriousperformance changes that would follow

0036-8075/82/l 112-0697$01.00/0 Copyright © 1982 AAAS

A Specific and Enduring Improvement inVisual Motion Discrimination

Abstract. Training improves the ability of human observers to discriminatebetween two similar directions ofmotion. This gradual improvement is specific to thedirection on which an observer is trained, and it endures for several months.Improvement does not affect motion perception generally, nor does it depend on

697

on Septem

ber 10, 2020

http://science.sciencemag.org/

Dow

nloaded from

)Apis melliferaIron-Containing Cells in the Honey Bee (DEBORAH A. KUTERBACH, BENJAMIN WALCOTT, RICHARD J. REEDER and RICHARD B. FRANKEL

DOI: 10.1126/science.218.4573.695 (4573), 695-697.218Science 

ARTICLE TOOLS http://science.sciencemag.org/content/218/4573/695

REFERENCES

http://science.sciencemag.org/content/218/4573/695#BIBLThis article cites 18 articles, 7 of which you can access for free

PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions

Terms of ServiceUse of this article is subject to the

is a registered trademark of AAAS.ScienceScience, 1200 New York Avenue NW, Washington, DC 20005. The title (print ISSN 0036-8075; online ISSN 1095-9203) is published by the American Association for the Advancement ofScience

1982 by the American Association for the Advancement of Science

on Septem

ber 10, 2020

http://science.sciencemag.org/

Dow

nloaded from