- Email: [email protected]
Biological Optics: Deep Reflections
Current Biology Vol 19 No 2 R78
research suggests that neglect arises when damage severs the anatomical connections and thus disrupts the functional interactions between parietal and frontal cortex. Several parallel parietal-frontal pathways exist, and damage to any of these tracts might induce neglect. The evidence to date has identified at least two tracts which when damaged give rise to neglect symptoms: a superior pathway inter-linking dorsal regions of parietal and frontal cortex, and a more inferior pathway connecting ventral parietal-frontal regions [5,7,8]. Differences among patients in the patterning and severity of both local cortical damage and parietal-frontal disconnection may account for symptom diversity, and also explain why an individual patient may be impaired on some tests of neglect but not on others. For example, in Koch et al.’s [2] study, hyper-activation of the parietal-motor pathway correlated with neglect severity on line and letter cancellation tasks. Although object naming improved after suppressive TMS, the behavioural change did not relate to the excitability change in that pathway. This dissociation may reflect important differences between the
clinical and experimental tests used to measure neglect. Line cancellation requires patients to search for targets in a cluttered space, a task known to rely on dorsal parietal-frontal interactions. Koch et al.’s [2] twin-coil TMS technique likely probes those connections. By contrast, object naming recruits more ventral pathways, whose activation state was not assessed. While object naming performance may have improved partly because repetitive TMS suppressed the spatial bias caused by dorsal hyperactivity, inter-regional stimulation spread may have altered excitability in more than one pathway. Combination approaches using functional and structural imaging together with novel TMS protocols, such as that used by Koch et al. [2], are beginning to tackle the challenge of understanding how local lesions disrupt large-scale brain network dynamics. The potential combination of diffusion imaging and TMS physiological connectivity probes offers a way to interrogate changes in the functioning of distinct parietal-frontal pathways after stroke and during recovery, promising a stimulating future for neglect research.
Biological Optics: Deep Reflections An image-forming optical system that is based on a mirror with an unconventional structure has recently been discovered in a deep-sea fish. Michael F. Land At depths between 500–1000m there is still some residual daylight from the surface, and many fish have large upward-pointing eyes which they use to spot the silhouettes of potential prey [1]. The other source of light in this zone is bioluminescence: light emitted by the luminous organs of a wide variety of both vertebrates and invertebrates, for defence, display or as lures to attract prey. Such light is best detected by looking downwards into the dark of the abyss, and accordingly many mid-water animals have some arrangement for scanning the water below them [2]. In fish this can take many forms. Bathylychnops
exilis, for example, has a secondary eye with its own lens and retina (Figure 1A) [3]. In Benthalbella infans and its relatives, there is a structure known as a lens pad, which redirects light from below through the main lens to an extension of the main retina [4]. And now Wagner et al. [5] have reported that, in another deep sea fish, Dolicopteryx longipes, a substantial region below the fish is imaged by a curved mirror onto a retina in an outgrowth of the main eye (Figure 1B). Whilst reflectors of various kinds are common throughout the animal kingdom, this is the first time an image-forming mirror has been demonstrated in a vertebrate.
References 1. Mort, D.J., Malhotra, P., Mannan, S.K., Rorden, C., Pambakian, A., Kennard, C., and Husain, M. (2003). The anatomy of visual neglect. Brain 126, 1986–1997. 2. Koch, G., Oliveri, M., Cheeran, B., Ruge, D., Gerfo, E.L., Salerno, S., Torriero, S., Marconi, B., Mori, F., Driver, J., et al. (2008). Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. Brain 131, 3147–3155. 3. Kinsbourne, M. (1977). Hemi-neglect and hemisphere rivalry. Adv. Neurol. 18, 41–49. 4. Hallett, M. (2007). Transcranial magnetic stimulation: a primer. Neuron 19, 187–199. 5. He, B.J., Snyder, A.Z., Vincent, J.L., Epstein, A., Shulman, G.L., and Corbetta, M. (2007). Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53, 905–918. 6. Corbetta, M., Kincade, M.J., Lewis, C., Snyder, A.Z., and Sapir, A. (2005). Neural basis and recovery of spatial attention deficits in spatial neglect. Nat. Neurosci. 8, 1603–1610. 7. Thiebaut de Schotten, M., Urbanski, M., Duffau, H., Volle, E., Levy, R., Dubois, B., and Bartolomeo, P. (2005). Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309, 2226–2228. 8. Bartolomeo, P., Thiebaut de Schotten, M., and Doricchi, F. (2007). Left unilateral neglect as a disconnection syndrome. Cereb. Cortex 17, 2479–2490.
Oxford Centre for Functional MRI of the Brain (FMRIB), John Radcliffe Hospital, University of Oxford, Oxford OX3 9DU, UK. E-mail: [email protected] DOI: 10.1016/j.cub.2008.11.038
Animals use reflectors for many purposes. Among butterflies, the brilliant blue wings of Morpho species and many others are used for sexual advertisement. In silvery fish, such as the herring, the reflecting scales are used for camouflage; this works because the light reflected from a fish’s flank is of similar intensity to the light that would have passed through the fish if it had not been there [6]. Mirrors are common in eyes as tapeta behind the retina; these reflect light back through the photoreceptors, giving them a second chance to capture photons. The eye-shine of cat eyes is familiar, but similar light-doubling arrangements are found in most nocturnal animals, from crocodiles and sharks to moths and spiders [7]. Mirrors can also act as image-forming optical systems. The eyes of scallops are the most
Dispatch R79
straightforward example. A concave mirror lining the hemispherical back of the eye focuses light back to a retina at the mirror’s focus, halfway between the mirror and its centre of curvature (Figure 1C). The retina contains off-responding cells, and when the image of a potential predator crosses them they fire, and the scallop either shuts or swims off [8]. This design is rare: up to now, only a small number of molluscs and crustaceans have eyes that are known to work on a similar principle. Its main drawback is that light has already passed once through the retina before being focused, so the effective image contrast is reduced to half that of a lens eye. A rather more complicated mirror-based optical system is found in the compound eyes of many decapod crustaceans — the prawns, crayfish and lobsters. Here, the optical elements are silvered boxes of jelly, with their faces at right angles to the eye surface (Figure 1D). This arrangement produces an image half-way out from the eye’s centre, which is where the retina is located [9]. Many other animals, notably krill and moths, have a similar ‘superposition’ arrangement, but using lens systems rather than mirrors [7]. From an optical point of view, the most interesting feature of the mirror in the eye of Dolichopteryx is that it is not a simple surface, but a stack of reflecting plates each making a slightly different angle with the surface supporting them (Figure 1D). In principle, a parabolic surface can form an image on the parabola’s axis (F in Figure 1F). However, for rays not parallel to the axis, the image quality rapidly deteriorates (grey triangle on Figure 1F) and ultimately becomes unusable. The arrangement shown in Figure 1D overcomes this to a large extent. The form of the supporting surface and the inclination of the mirror plates to this surface can be chosen to provide an image that is optimised over a wide angle. In their paper, Wagner et al. [5] show that this mirror can form a nearly flat image of good quality over the whole 48 field of view. They also show that, if the reflecting plates are made parallel to the surface, the image produced is very poor. It might be thought that tilting the mirror plates in this way would be difficult to achieve, but it does occur elsewhere in fish. The camouflage strategy of silvery fish only works if their sides are effectively plane mirrors, which
B
A
D
C
E
F
F
Current Biology Figure 1. Eyes with mirrors. In all panels, mirrors are shown in blue and retinae in red. (A) The double lens eyes of Bathylychnops exilis. (Based on [3].) (B) Double eye of Dolicopteryx longipes, with the lens eye pointing upwards, and the mirror eye pointing downwards. (Based on [5].) (C) Concave mirror optical system of a scallop. (Based on [8].) (D) Optical system of a decapod crustacean, in which each element of the compound eye is a square mirror box. (Based on [9].) (E) Imageforming reflector in which the reflecting plates make increasingly steep angles with the support surface. This is the mechanism of the reflector in (B), here shown inverted. (F) A half parabola will also form a point image at F, but for off-axis rays the image quality deteriorates rapidly (grey triangle).
means that they cannot conform to the rounded body of the fish. The reflecting platelets in the scales are indeed tilted systematically relative to the body surface, in such a way that the mirror surface appears flat [6].
The eye of Dolichopteryx longipes has only been described once before, and such fish are rarely caught. Wagner et al. [5] had only a single fresh specimen at their disposal, and it is impressive that they got as much from it as they did. The optics of
Current Biology Vol 19 No 2 R80
the reflecting eye had to be inferred from ray tracing, and although this is totally convincing it would be wonderful to find a way of actually seeing the image and assessing its quality directly. It would be good, too, to have more detailed information about the ultrastructure of the multilayer reflector itself. However, it may be several decades before this extraordinary fish turns up again. References 1. Denton, E.J. (1990). Light and vision at depths greater than 200 metres. In Light and Life in the
2.
3.
4.
5.
Sea, P.J. Herring, A.K. Campbell, M. Whitfield, and L. Maddock, eds. (Cambridge: Cambridge University Press), pp. 127–148. Land, M.F. (2000). On the functions of double eyes in midwater animals. Phil. Trans. R. Soc. B. 355, 1147–1150. Locket, N.A. (1977). Adaptations to the deep-sea environment. In The Visual System in Vertebrates. Handbook of Sensory Physiology VolVII/5, F. Crescitelli, ed. (Berlin: Springer Verlag), pp. 67–192. Locket, N.A. (2000). On the lens pad of Benthalbella infans, a scopelarchid deep-sea teleost. Phil. Trans. R. Soc. B. 355, 1167–1169. Wagner, H.-J., Douglas, R.H., Frank, T.M., Roberts, N.W., and Partridge, J.C. (2009). Dolichopteryx longipes, a deep-sea fish with a bipartite eye using both refractive and reflective optics. Curr. Biol. 19, 108–114.
6. Denton, E.J. (1970). On the organization of the reflecting surfaces in some marine animals. Phil. Trans. R. Soc. B. 258, 285–313. 7. Land, M.F., and Nilsson, D.-E. (2002). Animal Eyes (Oxford: Oxford University Press). 8. Land, M.F. (1965). Image formation by a concave reflector in the eye of the scallop, Pecten maximus. J. Physiol. 179, 138–153. 9. Vogt, K. (1980). Die Spiegeloptik des Flusskrebsauges. The optical system of the crayfish eye. J. Comp. Physiol. 135, 1–19.
Department of Biology and Environmental Biology, University of Sussex, Brighton BN1 9QG, UK. E-mail: [email protected] DOI: 10.1016/j.cub.2008.11.034
research suggests that neglect arises when damage severs the anatomical connections and thus disrupts the functional interactions between parietal and frontal cortex. Several parallel parietal-frontal pathways exist, and damage to any of these tracts might induce neglect. The evidence to date has identified at least two tracts which when damaged give rise to neglect symptoms: a superior pathway inter-linking dorsal regions of parietal and frontal cortex, and a more inferior pathway connecting ventral parietal-frontal regions [5,7,8]. Differences among patients in the patterning and severity of both local cortical damage and parietal-frontal disconnection may account for symptom diversity, and also explain why an individual patient may be impaired on some tests of neglect but not on others. For example, in Koch et al.’s [2] study, hyper-activation of the parietal-motor pathway correlated with neglect severity on line and letter cancellation tasks. Although object naming improved after suppressive TMS, the behavioural change did not relate to the excitability change in that pathway. This dissociation may reflect important differences between the
clinical and experimental tests used to measure neglect. Line cancellation requires patients to search for targets in a cluttered space, a task known to rely on dorsal parietal-frontal interactions. Koch et al.’s [2] twin-coil TMS technique likely probes those connections. By contrast, object naming recruits more ventral pathways, whose activation state was not assessed. While object naming performance may have improved partly because repetitive TMS suppressed the spatial bias caused by dorsal hyperactivity, inter-regional stimulation spread may have altered excitability in more than one pathway. Combination approaches using functional and structural imaging together with novel TMS protocols, such as that used by Koch et al. [2], are beginning to tackle the challenge of understanding how local lesions disrupt large-scale brain network dynamics. The potential combination of diffusion imaging and TMS physiological connectivity probes offers a way to interrogate changes in the functioning of distinct parietal-frontal pathways after stroke and during recovery, promising a stimulating future for neglect research.
Biological Optics: Deep Reflections An image-forming optical system that is based on a mirror with an unconventional structure has recently been discovered in a deep-sea fish. Michael F. Land At depths between 500–1000m there is still some residual daylight from the surface, and many fish have large upward-pointing eyes which they use to spot the silhouettes of potential prey [1]. The other source of light in this zone is bioluminescence: light emitted by the luminous organs of a wide variety of both vertebrates and invertebrates, for defence, display or as lures to attract prey. Such light is best detected by looking downwards into the dark of the abyss, and accordingly many mid-water animals have some arrangement for scanning the water below them [2]. In fish this can take many forms. Bathylychnops
exilis, for example, has a secondary eye with its own lens and retina (Figure 1A) [3]. In Benthalbella infans and its relatives, there is a structure known as a lens pad, which redirects light from below through the main lens to an extension of the main retina [4]. And now Wagner et al. [5] have reported that, in another deep sea fish, Dolicopteryx longipes, a substantial region below the fish is imaged by a curved mirror onto a retina in an outgrowth of the main eye (Figure 1B). Whilst reflectors of various kinds are common throughout the animal kingdom, this is the first time an image-forming mirror has been demonstrated in a vertebrate.
References 1. Mort, D.J., Malhotra, P., Mannan, S.K., Rorden, C., Pambakian, A., Kennard, C., and Husain, M. (2003). The anatomy of visual neglect. Brain 126, 1986–1997. 2. Koch, G., Oliveri, M., Cheeran, B., Ruge, D., Gerfo, E.L., Salerno, S., Torriero, S., Marconi, B., Mori, F., Driver, J., et al. (2008). Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. Brain 131, 3147–3155. 3. Kinsbourne, M. (1977). Hemi-neglect and hemisphere rivalry. Adv. Neurol. 18, 41–49. 4. Hallett, M. (2007). Transcranial magnetic stimulation: a primer. Neuron 19, 187–199. 5. He, B.J., Snyder, A.Z., Vincent, J.L., Epstein, A., Shulman, G.L., and Corbetta, M. (2007). Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53, 905–918. 6. Corbetta, M., Kincade, M.J., Lewis, C., Snyder, A.Z., and Sapir, A. (2005). Neural basis and recovery of spatial attention deficits in spatial neglect. Nat. Neurosci. 8, 1603–1610. 7. Thiebaut de Schotten, M., Urbanski, M., Duffau, H., Volle, E., Levy, R., Dubois, B., and Bartolomeo, P. (2005). Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309, 2226–2228. 8. Bartolomeo, P., Thiebaut de Schotten, M., and Doricchi, F. (2007). Left unilateral neglect as a disconnection syndrome. Cereb. Cortex 17, 2479–2490.
Oxford Centre for Functional MRI of the Brain (FMRIB), John Radcliffe Hospital, University of Oxford, Oxford OX3 9DU, UK. E-mail: [email protected] DOI: 10.1016/j.cub.2008.11.038
Animals use reflectors for many purposes. Among butterflies, the brilliant blue wings of Morpho species and many others are used for sexual advertisement. In silvery fish, such as the herring, the reflecting scales are used for camouflage; this works because the light reflected from a fish’s flank is of similar intensity to the light that would have passed through the fish if it had not been there [6]. Mirrors are common in eyes as tapeta behind the retina; these reflect light back through the photoreceptors, giving them a second chance to capture photons. The eye-shine of cat eyes is familiar, but similar light-doubling arrangements are found in most nocturnal animals, from crocodiles and sharks to moths and spiders [7]. Mirrors can also act as image-forming optical systems. The eyes of scallops are the most
Dispatch R79
straightforward example. A concave mirror lining the hemispherical back of the eye focuses light back to a retina at the mirror’s focus, halfway between the mirror and its centre of curvature (Figure 1C). The retina contains off-responding cells, and when the image of a potential predator crosses them they fire, and the scallop either shuts or swims off [8]. This design is rare: up to now, only a small number of molluscs and crustaceans have eyes that are known to work on a similar principle. Its main drawback is that light has already passed once through the retina before being focused, so the effective image contrast is reduced to half that of a lens eye. A rather more complicated mirror-based optical system is found in the compound eyes of many decapod crustaceans — the prawns, crayfish and lobsters. Here, the optical elements are silvered boxes of jelly, with their faces at right angles to the eye surface (Figure 1D). This arrangement produces an image half-way out from the eye’s centre, which is where the retina is located [9]. Many other animals, notably krill and moths, have a similar ‘superposition’ arrangement, but using lens systems rather than mirrors [7]. From an optical point of view, the most interesting feature of the mirror in the eye of Dolichopteryx is that it is not a simple surface, but a stack of reflecting plates each making a slightly different angle with the surface supporting them (Figure 1D). In principle, a parabolic surface can form an image on the parabola’s axis (F in Figure 1F). However, for rays not parallel to the axis, the image quality rapidly deteriorates (grey triangle on Figure 1F) and ultimately becomes unusable. The arrangement shown in Figure 1D overcomes this to a large extent. The form of the supporting surface and the inclination of the mirror plates to this surface can be chosen to provide an image that is optimised over a wide angle. In their paper, Wagner et al. [5] show that this mirror can form a nearly flat image of good quality over the whole 48 field of view. They also show that, if the reflecting plates are made parallel to the surface, the image produced is very poor. It might be thought that tilting the mirror plates in this way would be difficult to achieve, but it does occur elsewhere in fish. The camouflage strategy of silvery fish only works if their sides are effectively plane mirrors, which
B
A
D
C
E
F
F
Current Biology Figure 1. Eyes with mirrors. In all panels, mirrors are shown in blue and retinae in red. (A) The double lens eyes of Bathylychnops exilis. (Based on [3].) (B) Double eye of Dolicopteryx longipes, with the lens eye pointing upwards, and the mirror eye pointing downwards. (Based on [5].) (C) Concave mirror optical system of a scallop. (Based on [8].) (D) Optical system of a decapod crustacean, in which each element of the compound eye is a square mirror box. (Based on [9].) (E) Imageforming reflector in which the reflecting plates make increasingly steep angles with the support surface. This is the mechanism of the reflector in (B), here shown inverted. (F) A half parabola will also form a point image at F, but for off-axis rays the image quality deteriorates rapidly (grey triangle).
means that they cannot conform to the rounded body of the fish. The reflecting platelets in the scales are indeed tilted systematically relative to the body surface, in such a way that the mirror surface appears flat [6].
The eye of Dolichopteryx longipes has only been described once before, and such fish are rarely caught. Wagner et al. [5] had only a single fresh specimen at their disposal, and it is impressive that they got as much from it as they did. The optics of
Current Biology Vol 19 No 2 R80
the reflecting eye had to be inferred from ray tracing, and although this is totally convincing it would be wonderful to find a way of actually seeing the image and assessing its quality directly. It would be good, too, to have more detailed information about the ultrastructure of the multilayer reflector itself. However, it may be several decades before this extraordinary fish turns up again. References 1. Denton, E.J. (1990). Light and vision at depths greater than 200 metres. In Light and Life in the
2.
3.
4.
5.
Sea, P.J. Herring, A.K. Campbell, M. Whitfield, and L. Maddock, eds. (Cambridge: Cambridge University Press), pp. 127–148. Land, M.F. (2000). On the functions of double eyes in midwater animals. Phil. Trans. R. Soc. B. 355, 1147–1150. Locket, N.A. (1977). Adaptations to the deep-sea environment. In The Visual System in Vertebrates. Handbook of Sensory Physiology VolVII/5, F. Crescitelli, ed. (Berlin: Springer Verlag), pp. 67–192. Locket, N.A. (2000). On the lens pad of Benthalbella infans, a scopelarchid deep-sea teleost. Phil. Trans. R. Soc. B. 355, 1167–1169. Wagner, H.-J., Douglas, R.H., Frank, T.M., Roberts, N.W., and Partridge, J.C. (2009). Dolichopteryx longipes, a deep-sea fish with a bipartite eye using both refractive and reflective optics. Curr. Biol. 19, 108–114.
6. Denton, E.J. (1970). On the organization of the reflecting surfaces in some marine animals. Phil. Trans. R. Soc. B. 258, 285–313. 7. Land, M.F., and Nilsson, D.-E. (2002). Animal Eyes (Oxford: Oxford University Press). 8. Land, M.F. (1965). Image formation by a concave reflector in the eye of the scallop, Pecten maximus. J. Physiol. 179, 138–153. 9. Vogt, K. (1980). Die Spiegeloptik des Flusskrebsauges. The optical system of the crayfish eye. J. Comp. Physiol. 135, 1–19.
Department of Biology and Environmental Biology, University of Sussex, Brighton BN1 9QG, UK. E-mail: [email protected] DOI: 10.1016/j.cub.2008.11.034