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Responses of Primary Visual Cortical Neurons to Binocular Disparity

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Responses of Primary Visual Cortical Neurons to Binocular Disparity letters to nature resistance against pathogens and parasites in animals is scarce, and comes largely from studies on populations of farm or laboratory animals with highly modified genetic backgrounds (reviewed in Responses of primary visual ref. 1). Finally, because of the enormous amount known about Drosophila genetics, we suggest that the interactions between cortical neurons to binocular D. melanogaster and A. tabida may be a valuable model system for the study of the evolution of resistance and of the genetic basis of disparity without depth adaptation. M ......................................................................................................................... perception Methods Competitive ability of selected and control lines. Competitive ability was B. G. Cumming & A. J. Parker assessed by placing 15 second-instar larvae from the experimental lines (either University Laboratory of Physiology, Parks Road, Oxford OX1 3PT, UK control or selected insects) with 15 second-instar larvae from the tester stock ......................................................................................................................... (sparkling poliert, an eye-colour mutant) in agar-lined Petri dishes with The identification of brain regions that are associated with the variable amounts of larval medium. Four food levels were used: 0.4, 0.2, 0.1 or conscious perception of visual stimuli is a major goal in 0.05 ml of larval medium (25 g live baker’s yeast per 100 ml water), which neuroscience1. Here we present a test of whether the signals on represent weak to strong competition regimes. We recorded the number of neurons in cortical area V1 correspond directly to our conscious experimental and tester flies that survived, the development time to pupation perception of binocular stereoscopic depth. Depth perception and to adult eclosion, and female size and fluctuating asymmetry (wing requires that image features on one retina are first matched length). We performed 15 replicates of each combination of line and food level. with appropriate features on the other retina. The mechanisms Data analysis. Survival data were analysed using both a robust competition that perform this matching can be examined by using random-dot index (I) and a more sophisticated analysis using generalized linear modelling stereograms2, in which the left and right eyes view randomly techniques (II). For analysis (I) we calculated the competition index15, positioned but binocularly correlated dots. We exploit the fact logðe=ðt þ 1ÞÞ, where e is the number of experimental and t is the number of that anticorrelated random-dot stereograms (in which dots in one tester flies that survived in each replicate. The means of the competition index eye are matched geometrically to dots of the opposite contrast in for the eight lines were calculated and differences between selected and control the other eye) do not give rise to the perception of depth3 because lines tested using the t-test with unequal variances. For analysis (II) the the matching process does not find a consistent solution. Anti- untransformed survival data for the experimental flies were analysed in a correlated random-dot stereograms contain binocular features generalized linear model with binomial error variances, but using quasi- that could excite neurons that have not solved the correspondence likelihood estimation to account for overdispersion17. The numbers of tester problem. We demonstrate that disparity-selective neurons in V1 flies surviving was used as a covariate and significance assessed by nesting lines signal the disparity of anticorrelated random-dot stereograms, within control or selection treatments (giving an F-statistic with one and six indicating that they do not unambiguously signal stereoscopic degrees of freedom). Examination of the distribution of residuals supported the depth. Hence single V1 neurons cannot account for the conscious choice of model. The results of the two statistical analyses were in broad perception of stereopsis, although combining the outputs of many agreement (values in the text are from analysis (II)), with P for (I) given first: V1 neurons could solve the matching problem. The accompanying 0.4 ml, P . 0:1, P . 0:1; 0.2 ml, P . 0:1, P . 0:1; 0.1 ml, P ¼ 0:033, paper4 suggests an additional function for disparity signals from P ¼ 0:011; 0.05 ml, P ¼ 0:066, P ¼ 0:061. The data for size and development V1: they may be important for the rapid involuntary control of time were analysed using the appropriate general linear models equivalent to vergence eye movements (eye movements that bring the images on analysis (II). the two foveae into register). When the image of an object falls on different locations on the Received 25 March; accepted 8 July 1997. two retinae, this binocular disparity gives rise to a sensation of depth 1. Read, A. F. et al.inEcology of Infectious Diseases in Natural Populations (eds Grenfell, B. T. & Dobson, A. P.) 450–477 (Cambridge Univ. Press, 1995). (stereopsis). This process requires that an image feature on one 2. Partridge, L. & Fowler, K. Direct and correlated responses to selection on age at reproduction in retina be matched with an appropriate feature on the other retina, Drosophila melanogaster. Evolution 46, 76–91 (1992). even though there are inevitably similar features nearby offering 3. Rose, M. R. Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38, 1004–1010 (1984). potential matches. This problem is particularly apparent in 4. Salt, G. The Cellular Defence Reactions of Insects (Cambridge Univ. Press, 1970). random-dot stereograms (RDS), where there are many identical 5. Gupta, A. P. in Comprehensive Insect Physiology, Biochemistry and Pharmocology, Vol. 3 (eds Kerkut, G. A. & Gilbert, L. I.) 401–451 (Pergamon, Oxford, 1985). dots in both images. Of course it is not necessary to consider false 6. Strand, M. R. & Pech, L. L. Immunological basis for compatibility in parasitoid-host relationships. matches in RDS on a dot-by-dot basis—spatial filtering of the Annu. Rev. Entomol. 40, 31–56 (1995). image before matching can substantially reduce the number of false 7. Godfray, H. C. J. Parasitoids, Behavioral and Evolutionary Ecology, (Princeton Univ. Press, NJ, 1994). 5 8. Carton, Y. & Bouletreau, M. Encapsulation ability of Drosophila melanogaster: a genetic analysis. Dev. matches . However, this filtering alone is insufficient to solve the Comp. Immunol. 9, 211–219 (1985). correspondence problem and further computation is required to 9. Carton, Y. & Nappi, A. J. The Drosophila immune reaction and the parasitoid capacity to evade it: genetic and coevolutionary aspects. Acta Oecol. 12, 89–104 (1991). eliminate false matches. Consideration of the overall pattern of 10. Henter, H. J. & Via, S. The potential for coevolution in a host-parasitoid system. 1. Genetic variation disparities can indicate which potential matches form a globally within an aphid population in susceptibility to a parasitic wasp. Evolution 49, 427–438 (1995). consistent pattern, and many computer algorithms achieve this5,6. 11. Hughes, K. & Sokolowski, M. B. Natural selection in the laboratory for a change in resistance by Drosophila melanogaster to the parasitoid wasp Asobara tabida. J. Insect Behav. 9, 477–491 (1996). Although single neurons in V1 have long been known to signal 12. Kraaijeveld, A. R. & van der Wel, N. N. Geographic variation in reproductive success of the parasitoid the disparity of a stimulus7,8, their role in stereo matching is unclear. Asobara tabida in larvae of several Drosophila species. Ecol. Entomol. 19, 221–229 (1994). 13. Kraaijeveld, A. R. & van Alphen, J. J. M. Geographical variation in encapsulation ability of Drosophila If they are directly responsible for the conscious perception of melanogaster larvae and evidence for parasitoid-specific components. Evol. Ecol. 9, 10–17 (1995). depth, they should respond only when matches within the receptive 14. Lewonton, R. C. The effects of population density and composition on viability in Drosophila field are registered as globally correct. If binocular neurons respond melanogaster. Evolution 9, 27–41 (1955). 15. Santos, M., Fowler, K. & Partridge, L. On the use of tester stocks to predict the competitive ability of equally well to false matches at appropriate disparities, then further genotypes. Heredity 69, 489–495 (1992). processing (presumably outside V1) is required to account for the 16. Atkinson, W. D. A field investigation of larval competition in domestic Drosophila. J. Anim. Ecol. 48, 91–102 (1979). psychophysical ability to discard false matches. 17. McCullagh, P. & Nelder, J. A. Generalized Linear Models 2nd edn (Chapman & Hall, London, 1989). Whether or not disparity-selective neurons respond only to correct matches is an open question. It has been demonstrated Acknowledgements. We thank J. van Alphen, G. Boskamp, A. Burt, D. Ebert, J. Ellers, M. Fellowes, A. James, A. Leroi, J. McCabe, A. Orr, L. Partridge, A. Read, M. Rees and J. Werren for help and advice. that some V1 complex cells display disparity selectivity to dynamic RDSs and it was concluded that these neurons signal ‘‘the correct Correspondence and requests for materials should be addressed to H.C.J.G. (e-mail: [email protected]). binocular matches among a multitude of false matches ... (global Nature © Macmillan Publishers Ltd 1997 280 NATURE | VOL 389 | 18 SEPTEMBER 1997 letters to nature Figure 1 Example stereograms. The pair formed by the central image and the left Figure 2 Responses of a model complex cell to RDS. The model neuron was image forms a C-RDS showing a central circular patch standing out in depth tuned to zero-disparity stimuli. Filled symbols show responses to C-RDS, open (shown for cross-eyed fusion). The pair formed by the central image and the right symbols show responses to A-RDS. Both axes have arbitrary units. The model image is an A-RDS, and appears rivalrous with no consistent depth. Note that the neuron had subunits that were matched in their spatial and temporal properties, right image is an exact copy of the left image in which the dot brightnesses have so the two tuning curves are exact mirror images.
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