BRIAN ROGERS VISUAL PERCEPTION

On course for collision? Information about the time-to-collision is provided by the rate

of dilation of the retinal image. We now have evidence for mechanisms in the pigeon visual system that signal time-to-collision.

The ability to extract information about the three-dimen- sional characteristics of the surrounding visual environ- ment is extremely useful in order to control many aspects of behaviour. There are, however, some behaviours and activities for which the important controlling variable is temporal rather than spatial. An obvious example in human behaviour is ball-catching. To catch a ball suc- cessfully, the closing movements of the tigers need to be initiated before the ball reaches the hands and thus WC need to be able to estimate, in advance, the remaining time before the ball reaches us. This could be done by es- timating the ball’s absolute distance and dividing it by an estimate of its approach velocity: velocity = distance/time and hence time = distance/velocity.

An alternative strategy, which was first suggested by Gib- son [l] and has been investigated extensively by Let [2] over the last twenty years, is to use the ‘rate of dilation’ of the image of the approaching objcyt. A rapidly approach- ing object that is a large distance away may reach the ob- server at the same time ;1s a more slowly moving object that is much closer. Simple geometry shows that in these two situations the rates of dilation of the image will be the same. From this, Lee has shown that there is a sim- ple optic parameter ~(tau) -- defined as the inverse of the mte of dilation of the image - which specifies the ‘time-to-collision’ of the object with the ob.server, as long as the closing velocity between object and observer re- mains constant. The optic parameter T is not only useful for estimating the time before a moving obiect reaches an observer; if the observer is moving the image of his sur- roundings dilates, and the local rate of dilation provides an estimate of the time before the observer reaches that point in the surrounding environment.

Is there any evidence to suggest that animals are able to use the rate of dilation of the retinal image to control the timing of their actions? In a classic study of long-jumpers approaching the take-off point for their jump, 1~ CY al. [3] showed that the length of stride in the run up is not const;Ult (as the long-jumpers themselves believed), but instead is adjustcti during the final few strides so as to position the last stride as close as possible to the take- off point. Although this result provides good evidence for the visual control of action it does not, by itself, protide conclusive evidence for the use of f, as the adjustment might have been based on visual information about the ab.sotutc distance to the take-off board. Subsequent ex- periments by Schiff and Detwiler [4] and McLeod and Ross [S] presented subjects with visually expanding im- ages on a two-dimensional projection screen at a fixed distance from the obsenYcr in order to eliminate the

Volume 2 Number 7 1992

possibility of computing time-to-collision indirectly from speed and chance estimates. Their results show that the observers’ judgements of how soon an approaching ob- ject will reach them or how soon the obsemer will reach a point in the expanding image of the three-dimensional sccnc both vary inversely with the rate of dilation as pre- dicted by the ‘I: hypothesis. These experiments are not conclusive either, however, because the observers could have used a cognitive strategy, based on how rapidly the image dilates on the screen, and responded accordingly.

The situation becomes more complicated when the CIOS- ing velocity between the object and ob,server is not con- stant, For example, if a bird is accelerating under gravity, it will reach an object or surface sooner than the instan- taneous rate of dilation would predict and hence the ‘z: parameter will always provide an overestimate of the ac- tual time to contact. llnder conditions of deceleration, such as when the same bird is landing on a branch, the mte of dilation (and hence the t parameter) will provide an underestimate of the actual time to contact. Lee [6] has shown that actual time to contact can still be determined if the animal could monitor both the time to contact, parameter t, and its temporal derivative, 6t/i% or i. Alternatively, the animal might adopt the simpler r mar- gin strategy, obtaining an estimate of T at the last possible momcnr, when the effect of acceleration in overestimat- ing the acl~~d time to contact will be minimal.

In a study of the behaviour of gannets diving for lish, IE and Reddish [7] showed that the point at which the gan- nets folded back their wings before reaching the water ws best modelled by assuming the gannets adopted such a f margin strategy. In a more recent study of the approach behaviour of humming birds, Ixe et al. [8] have suggested that the ‘braking’ response is con- trolled by the rate of change of the t parameter - i+ Humans &so appear to be able to respond appropri- ately when the approaching object is accelerating. Lze and colleagues [9], for example, have reported that the performance of human subjects in punching a ball that was accelerating down towards them under gravity wds best modelltd in terms of a f margin strategy, based on an estimate of ‘I: obtained around 100ms before the ball reached them.

A$ a result of these studies, we now have good evidence to suggest that humans and other animals are able to USC the rate of dilation of retinal images as a source of information about the time-to-collision between object and obsemer. Until recently, however, our knowledge of the nature and location of the brain mechanisms involved

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was very limited. A recent paper by Wang and Frost 110) has provided some clues. They pre.sented an optic flow pattern, which simulated an approaching soccer batI witi constant velocity, on a two-dimensional projection screen in front of a pigeon and simultaneously recorded from single cells in the nucleus rotundus (a major midbrain nucleus in the tectofugal pathway of the pigeon).

Some 24 out of 145 ceils in the pigeon nucleus rotun- dus responded maximaliy to a Iooming stimuhrs that was on an approach path towards the pigeon These neurons had extremely large receptive fields, covering 100 degrees or more of the visual field, but they failed to give a response when the simulated object moved along a fronto-parallel trajectory (in the plane of the projection screen) or on a trajectory that was towards the pigeon but not on a ‘collision’ path. Indeed, Wang and Frost re- ported that three of these cells were exquisitely tuned to the direction of approach with tuning ctuves of * 3+3 degrees. These cells appeared to be highly selective for the optic flow produced by an object that approached the bird and gave little or no response when the whole of the visual image expanded, as would be produced by its own locomotion.

Control experiments .by Wang and Frost showed that the responses of the cells did not vay with either the size of the simulated approaching object (between lO-5Ocm diameter) or the speed of its approach (be- tween 150-750cms- *). It is clearly important that the cells show such invariances in their response properties in order to be sure that they are responding to the rate of dilation of the stimulus pattern and not to some other characteristic of the display.

In addition to their selectivity for the direction of ap- proach, the neurons studied by Wang and Frost also appeared to signal the precise time before an impend- ing collision. Each of the cells tested showed a rapid increase in its rate of firing at a particular time (be- tween 800-l 400 ms) before contact. This suggests that those cells might be involved in ttiggering an avoidance response during the last second before collision. Ad- ditional evidence for this hypothesis comes from the fact that there was an increase in both the heart rate and the muscle activity shortly after the visual response to the looming stimulus. Moreover, both responses

occurred only when the stimulus was on a precise cob sion trajectory. The results of Wang and Frost provide the first good ev- idence that there are mechanisms in the pigeon visual system that are capable of extracting the rate of di- lation of an expanding image on the pigeon’s retina independently of the velocity and size of the approaching object, and they raise the intriguing possibility that these ceUs may pray a functional role in the initiation of avoid- ance behaviour. One unanswered question, however, is whether the neurons in the nucleus rotundus are sim- ply responding to ‘I: (given by the instantaneous rate of dilation of the image) or instead to the actual tirne-to- collision, which would require estimates of both t and t, as indicated earlier. To answer this question, Frost and Lee are presently planning to monitor the same cells’ responses to a simulated soccer ball that is either accelerating or decelerating during its approach to the pigeon.

References I< GLB%N JJ: ‘Ihe Emlo@al Appmcb to KsuaI Perceprion Boston:

Houghton Mimin, 1979. 2. i&E DN: The Optic fhW fiekk the foundation of vision. f%ifos

Trans R Sot Land /Mel] 1980, B2!30:16!9-179. 3. LEE DN, IJSHMAN JR, THOMPSON Jk Regulation of gait in long

jumping. J Exp Pq&ol Human Percqth and Per@mance 1982, 9A48-459.

4. SCHIFF W, DEIWUR ML Information used in judghg impend- ing collision. Perception 1979, 8:647-65$.

5. MCLEOD RW, Ross H: Optic flow and cognitive factors in time-to-collision estimates. Perceprion 1983, 12:417-424.

6. LEE DN: A theory of visual control of braking based on in- formation about time-twcoliision. Perception 1976, 5:437-459.

7. I&E DN, RELISH PE: Flwntneting gannets: a paradigm of eco- logical optics. ktUFC 1981, 293293294.

8 LEE DN, REDDISH PE, RMND DT: Aerial docking by humming birds. Ivutuissetiflen 1991, 78:526527.

9. LEE DN, YOUNG DS, LOUGH S, CIAITON TMH: Visual riming in hitting an accelerating ball. QJ f5p Psychos 1983, 35~333-346.

10. WIG Y, FROST BJ: Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nancre 1992, 356236-238.

Brian j. Rogers, Department of Experimental Psychology, University of Oxford, Oxford, OX1 3UD, UK.

372 @ 1992 Current Biology