Temporal events in cyclopean vision ( perception /

The majority of neurons in the primary visual cortex of primates can be activated by stimulation of either eye; moreover, the monocular receptive fields of such neurons are located in about the same region of visual space. These well-known facts imply that binocular convergence in visual cortex can explain our cyclopean view of the world. To test the adequacy of this assumption, we examined how human subjects integrate binocular events in time. Light flashes presented synchronously to both eyes were compared to flashes presented alternately (asynchronously) to one eye and then the other. Subjects perceived very-low-frequency (2 Hz) asynchronous trains as equivalent to synchronous trains flashed at twice the frequency (the prediction based on binocular convergence). However, at higher frequencies of presentation (4-32 Hz), subjects perceived asynchronous and synchronous trains to be increasingly similar. Indeed, at the flicker-fusion frequency ( 50 Hz), the apparent difference between the two conditions was only 2%. We suggest that the explanation of these anomalous findings is that we parse visual input into sequential episodes. The singleness of binocular vision is so self-evident that it is easy to overlook its monocular origins. Although binocular cortical neurons are generally thought to be the neural substrate of cyclopean perception (1, 2), very little is known about how monocular information is actually united. We were stimulated to consider this issue by a provocative experiment carried out by Charles Sherrington nearly a century ago (3, 4). Sherrington used the measure of critical flicker-fusion (i.e., the minimum frequency under specified conditions at which a flashing light is perceived as providing continuous illumination) to explore the nature of binocular convergence. He reasoned that if monocular information is united at a single neural locus (the sensory equivalent of the final common pathway that he had established for the mammalian motor system), then the critical flicker-fusion frequency should be reduced to about half the normal value when light flashes are presented alternately to the two eyes (see Fig. 1). (The flash rate here and subsequently refers to the rate presented to one eye). In the event, Sherrington found only a small difference (2%) between the critical flicker-fusion frequency in the two experimental conditions. He therefore concluded that the views of the two eyes must be united "psychically" by a mechanism that lay outside the province of conventional physiology (refs. 3 and 4; see, also, refs. 5 and 6). These experiments, with minor technical differences, were repeated several decades later by investigators who found a greater (10%) reduction of the critical flicker-fusion frequency in the asynchronous (i.e., out of phase) mode of presentation (7-10). Based on this outcome, C. H. Baker (11) concluded that Sherrington's interpretation was unwarranted. More recently still, Cavonious (12) has also disputed Sherrington's conclusion (although not his data), The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. 3689 based on his demonstration of binocular interactions in sensitivity to flicker modulation. To reexamine this contentious issue, we constructed an apparatus that could deliver stroboscopic flashes independently to the two eyes at rates and in sequences controlled by a computer (Fig. 1). In our first set of experiments, we essentially repeated the experiments of Sherrington (3, 4) [and Baker et al. (7-11)] on flicker-fusion with an improved paradigm (Fig. 1). The critical flicker-fusion frequency was defined as the rate at which a 1-sec train of light flashes was perceived as continuous illumination in 50% of the trials. For the 20 adult subjects tested, the mean critical flicker-fusion frequency for synchronous presentations was 47.3 ± 1.8 Hz (mean ± SEM), whereas for asynchronous presentations it was 46.3 ± 1.9 Hz (Fig. 2). Thus each of the subjects perceived flicker-fusion in the asynchronous condition at frequencies that were about the same as those that produced flicker-fusion with synchronous presentation to the two eyes. This result is identical to that reported by Sherrington. We next examined the perception of dichoptic stimulation at lower frequencies using a binocular matching paradigm to indicate whether or not paired trains of flashes produced the same percept (Fig. 3). As in the experiments on flicker-fusion, one member of the pair consisted of synchronous dichoptic flashes and the other of asynchronously presented flashes. Asynchronous trains at each of several frequencies (2, 4, 8, 16, and 32 Hz) were paired with a range of synchronous trains, such that the extremes gave rise to obvious differences in the perceived flicker rate (Fig. 3A). Trains of light flashes presented asynchronously to the two eyes at very low frequencies (2 Hz) were usually seen as identical to synchronous presentations at twice the rate (the result expected on the basis of monocular convergence) (Fig. 3B). However, at only slightly higher frequencies of presentation (4 Hz) and continuing to the highest rate tested (32 Hz), asynchronous and synchronous flashes presented at the same rate were increasingly judged to be the same. Thus, with increasing flash rate, the ratio of the asynchronous to synchronous presentation rate that gave rise to the same perception diminished from two to a value very near one at flicker-fusion. Moreover, fewer and fewer asynchronous presentations were seen as identical to synchronous presentations at twice the rate. Evidently, asynchronously presented light flashes begin to be conflated when the interval between successive stimuli to the two eyes is less than several hundred milliseconds. In short, a temporal limitation in the perception of dichoptically presented flashes is apparent at frequencies far less than the critical flicker-fusion frequency. How then should one regard Sherrington's conclusion that the two monocular views are elaborated independently and that this information is united only psychically? In light of the modern knowledge that 80% or more of neurons recorded from primate visual cortex, even under anesthesia, respond to stimulation of both eyes (1), the first part of Sherrington's interpretation is wrong in the sense that information from the two eyes is unequivocally brought together in VI. Nonetheless, the results obtained nearly a century ago on flicker-fusion, which we confirm, do present a profound puzzle. If binocular 3690 Neurobiology: Andrews et al. Visual Perception Binocular Cortical Circuitry / \ Right Eye Q A Aperture -i--Filter -/ Synoptophore 0 Left Eye A, Synchronous Presentation Train of flashes | l | | l I | to right eye l l1 1 Train of flashes l l I I I I I to left eye | 1 Asynchronous Presentation Train of flashes I I I I I I I to right eye 11 1 _ Train of flashes l I I I I I | to left eye l l1 1 time Computer FIG. 1. Diagram of the dichoptic presentation of light flashes. (Left) A computer program triggered two stroboscopic light sources (30-tLsec flash; 15 W; Monarch Instruments, Amherst, NH). The intensity of the light from the strobes was adjusted by neutral density filters to ensure equal photopic illumination of each eye from a modified synoptophore (Oculus type 58100, Wetzlar, Germany). Alignment of the monocular views was achieved by adjusting the arms of the synoptophore for each subject until the two images were exactly superimposed. During the trials, a low level of constant illumination allowed subjects to fixate and thereby maintain fusion of the monocular views between flashes. Thus when the two monocular images were superimposed, subjects saw a dimly illuminated circular field subtending 1.5° that was periodically the source of flashing light. (Right) The two types of dichoptic presentation-synchronous or asynchronous-are diagrammed. Note that the frequency of synchronous or asynchronous flash presentation refers to the rate received by one eye. D/A, digital/analog. )--O--O-.--"0-. -Syr oAs' 'IAM nchronous ynchronous