NEWS & VIEWS NE UROSCIENCE

Updating views of visual updating Our brains create a stable view of the world even though our eyes dart around. A study of how the brain might compensate for eye movements reveals an unexpected twist in the vision-stabilizing mechanism. See Letter p.504 JOHN A. ASSAD

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ision is the great illusionist. Although scenes before our eyes seem vivid and detailed, the part of the eye dedicated to high-acuity vision, the fovea, can cover only a narrow sliver of visual space — little more than the breadth of a thumbnail held at arm’s length. Vision seems so detailed because we constantly move our eyes to scan the highacuity fovea across a scene. Saccades — quick, jerky movements of the eyes — occur several times per second, filling in the perceptual fogginess of the visual periphery. Given this perpetual motion of the eyes, how the visual world looks so stable is an enduring mystery. The retina responds whenever the visual scene ‘slips’ across its surface, and is thus unable to distinguish between the scene flashing in front of the eyes (for example, a speeding train at a railway crossing) or the eyes rushing across the scene. The brain, however, generates eye movements, and thus could perceptually compensate for saccades1. On page 504 of this issue, Zirnsak et al.2 offer insight into how this compensation could occur. In 1992, the neuroscientist Michael Goldberg and his colleagues suggested a potential neuronal mechanism for eye-movement compensation3. These researchers studied neurons in the macaque monkey’s lateral parietal cortex, a part of the brain that serves as a bridge between vision and eye movements. Parietal neurons, like other visual neurons, have a receptive field (RF), a circumscribed part of the visual field for which visual stimuli activate electrical responses (Fig. 1). These RFs are defined relative to the fixation position (the point in visual space where the fovea is focused when eyes are stationary), and are usually considered spatially fixed relative to that position, reflecting the convergent hard-wired inputs to the neurons that ultimately stem from the retina. Thus, if the fixation position is displaced by a saccade, the RF should ‘move’ as well, in lockstep with the fixation position. However, Goldberg and co-workers made the important discovery that parietal RFs are more fluid around the time of saccades: when monkeys made saccades to a point on a computer screen, even before the eyes moved, the neurons could be activated by a spot of light

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Figure 1 | Movement of receptive fields.  a, Visual neurons have a receptive field (RF), a region of the visual field for which stimuli activate electrical responses. RFs are defined relative to the position fixated upon by the fovea, the tiny area of the eye that provides high-acuity vision. Here, the positions of three RFs are shown when the fovea is fixated at the red circle. b, After the fovea establishes fixation at a new point, the RFs move in lock-step with the new fixation position. Previous studies suggested that RFs shift to their new positions before the eyes move, a process known as predictive remapping. c, Zirnsak et al.2 report that the RFs transiently shift to the upcoming fixation point itself, instead of to the future RF locations.

that fell at the future position of the RF relative to the upcoming fixation point after the saccade. The researchers thus suggested that the RF was “updated” or “remapped” to the new position, perhaps to compensate perceptually for the upcoming eye movement. Similar spatial updating was subsequently found in other brain structures that have mixed visual and oculomotor (eye-movement) function, such as the frontal eye fields4 (FEFs) and the superior colliculus5, suggesting a common compensatory mechanism. A strongly held notion about the spatialupdating hypothesis is that the brain’s entire representation of the visual field rigidly translates in preparation for the abrupt movement of the eyes. However, in the original studies of spatial updating, visual stimuli were focused almost exclusively on the expected up­coming location of the RF. Zirnsak and colleagues have now widened the net in the simplest way imaginable: they presented visual stimuli to macaque monkeys not only at the up­coming (post-saccade) location of the RF of FEF neurons, but at various positions all over a

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computer screen, to map the entire RF. Surprisingly, when the full RFs were revealed, the authors found that these fields did not rigidly translate before the eye movement, but instead transiently shifted en masse towards the location of the upcoming saccade target (Fig. 1c; see also Fig. 3a of the paper2). Some of the shifts of individual RFs were substantial, up to 18 degrees of visual angle. Moreover, in the few cases in which the original RF was located farther away from the original fixation point than the saccade target (as measured along the direction of the saccade), the shift in the RF to the saccade-target location was actually in the opposite direction to that expected for a rigid translation of the RF relative to the fovea. The discovery that RFs collapse onto the saccade target is drastically different from the original spatial-updating hypothesis. So why did the authors of the original studies find neuronal responses at the upcoming position of the RF? In fact, the RFs of neurons in the FEF (and related visual–oculomotor structures) are quite large, so even if the RFs

NEWS & VIEWS RESEARCH collapsed to the saccade target, the fringes of many of those RFs would have probably overlapped with the upcoming RF location, and would thus respond to stimuli at that location. Indeed, in the original studies, responses at the upcoming RF location were often quite weak, which is consistent with the typically weaker responses at the periphery of RFs. Zirnsak and colleagues’ findings raise many issues. For one, RF shifts to a saccade target resemble the RF shifts that occur towards targets on which our attention is focused, even if the eyes do not move6,7. The two phenomena are probably related, inasmuch as shifts of attention to targets of interest precede eye movements. In this perspective, visual stability during saccades could result from the fact that

we effectively ignore those parts of the visual scene that are away from the saccade target. Moreover, spatial–perceptual distortions are known to occur owing to attention shifts and eye movements. These could be interesting phenomena to test further in monkeys, which can signal complex perceptions in experimental settings. More studies will also be needed to understand the cellular mechanisms of rapid RF modulation before saccades. But for experts and non-experts alike, Zirnsak et al. provide us with a valuable lesson: interesting things are often revealed when we search for our proverbial lost keys away from the streetlight. ■ John A. Assad is at the Center for Neuroscience and Cognitive Systems, Istituto

S OL A R SYSTEM

Stranded in no-man’s-land The discovery of a second resident in a region of the Solar System called the inner Oort cloud prompts fresh thinking about this no-man’s-land between the giant planets and the reservoir of comets of long orbital period. See Letter p.471 candidates have been found2–4, Sedna had remained the solitary confirmed member of a proposed inner Oort cloud beyond 70 au. On page 471 of this issue, Trujillo and Sheppard report5 the discovery of an object, called 2012 VP113, which joins Sedna as the second confirmed member of the inner Oort cloud. The finding solidifies the existence of a population of icy bodies probably ranging in size from a few to a thousand kilometres. To all intents and purposes, in the current architecture of the Solar System, Sedna and 2012 VP113 should not be there. These objects are in a no-man’s-land between the giant planets and the Oort cloud where nothing

MEGAN E. SCHWAMB

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decade after its discovery, Sedna1 still remains one of the strangest objects in the Solar System. This remote icy body is on a highly eccentric orbit that extends to about 1,000 astronomical units (au; 1 au is the mean Earth–Sun distance) and has a peri­helion (point of closest approach to the Sun) of 76 au. Its orbit is well beyond the reach of Neptune, which is located at 30 au, and is a long way from the edge of the Solar System where the Oort cloud, the reservoir of long-orbital-period comets, resides at about 10,000 au. Although other potential

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Figure 1 | The inner Oort cloud.  Trujillo and Sheppard5 have detected an object, called 2012 VP113, that joins Sedna as the second confirmed body of the inner Oort cloud, a region believed to lie between the disk-shaped Kuiper belt of icy bodies and the spherical Oort cloud of long-orbital-period comets. Sedna

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in the known configuration of the modernday Solar System could have emplaced them. Effectively frozen in place and untouched as the Solar System evolved to its present state, their orbits preserve the dynamical signature of whatever event scattered these bodies to such distances and detached them from the giant-planet region. With Sedna’s discovery in 2003, several formation mechanisms were put forth, each predicting different orbital distributions of inner Oort cloud objects. But with only a single object, it was impossible to unambiguously distinguish between the different hypotheses. Proposed mechanisms to explain the origin of the inner Oort cloud include the scattering of planetesimals (the building blocks of planet formation) by a distant planet beyond Neptune that may have been ejected from our Solar System, or by the passage of a single star, located at between 500 and 1,000 au, early on in the Solar System’s history6,7. The preferred mechanism is the gravitational scattering of leftover planet­esimals from close encounters between the nascent Sun and other members of its birth star cluster, which would have contained between 10 and 1,000 stars6,8–10. Most stars are born in stellar nurseries that dissolve within a few million years. At the present age of the

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1. von Helmholtz, H. A Treatise on Physiological Optics (transl. Southall, J. P. C.) (Dover, 1963). 2. Zirnsak, M., Steinmetz, N. A., Noudoost, B., Xu, K. Z. & Moore, T. Nature 507, 504–507 (2014). 3. Duhamel, J. R., Colby, C. L. & Goldberg, M. E. Science 255, 90–92 (1992). 4. Umeno, M. M. & Goldberg, M. E. J. Neurophysiol. 78, 1373–1383 (1997). 5. Walker, M. F., Fitzgibbon, E. J. & Goldberg, M. E. J. Neurophysiol. 73, 1988–2003 (1995). 6. Connor, C. E., Preddie, D. C., Gallant, J. L. & Van Essen, D. C. J. Neurosci. 17, 3201–3214 (1997). 7. Womelsdorf, T., Anton-Erxleben, K., Pieper, F. & Treue, S. Nature Neurosci. 9, 1156–1160 (2006).

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Italiano di Tecnologia, Rovereto 38068, Italy, and the Department of Neurobiology, Harvard Medical School, Boston, Massachusetts. e-mail: [email protected]

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Oort cloud (becomes spherical beyond about 5,000

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is roughly 1,000 km across, whereas 2012 VP113 is estimated to be about 400 km in diameter. Perihelion is the orbital point of closest approach to the Sun; aphelion is the orbital point farthest from the Sun; 1 au is the mean Earth–Sun distance. Objects in this diagram are not to scale. (Figure adapted from ref. 12.) 2 7 M A RC H 2 0 1 4 | VO L 5 0 7 | NAT U R E | 4 3 5

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Neuroscience: Updating views of visual updating.

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