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N K Logothetis

Publications and source records attributed to N K Logothetis.

18 recordsLinked to original sources

Single units and conscious vision.

Figures that can be seen in more than one way are invaluable tools for the study of the neural basis of visual awareness, because such stimuli permit the dissociation of the neural responses that underlie what we perceive at any given time from those forming the sensory representation of a visual pattern. To study the former type of responses, monkeys were subjected to binocular rivalry, and the response of neurons in a number of different visual areas was studied while the animals reported their alternating percepts by pulling levers. Perception-related modulations of neural activity were found to occur to different extents in different cortical visual areas. The cells that were affected by suppression were almost exclusively binocular, and their proportion was found to increase in the higher processing stages of the visual system. The strongest correlations between neural activity and perception were observed in the visual areas of the temporal lobe. A strikingly large number of neurons in the early visual areas remained active during the perceptual suppression of the stimulus, a finding suggesting that conscious visual perception might be mediated by only a subset of the cells exhibiting stimulus selective responses. These physiological findings, together with a number of recent psychophysical studies, offer a new explanation of the phenomenon of binocular rivalry. Indeed, rivalry has long been considered to be closely linked with binocular fusion and stereopsis, and the sequences of dominance and suppression have been viewed as the result of competition between the two monocular channels. The physiological data presented here are incompatible with this interpretation. Rather than reflecting interocular competition, the rivalry is most probably between the two different central neural representations generated by the dichoptically presented stimuli. The mechanisms of rivalry are probably the same as, or very similar to, those underlying multistable perception in general, and further physiological studies might reveal much about the neural mechanisms of our perceptual organization.

Animals

Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex.

Saccadic eye movements in primates continually shift the location at which a given stimulus strikes the retina. Even during periods of steady fixation, microsaccades frequently jerk the center of gaze by small but resolvable distances, yet perception remains stable and continuous, uninterrupted by sudden jumps or shifts. The effect of such fixational eye movements on the activity of single neurons was examined in several regions of the visual cortex in macaque monkeys. We found that the firing of many neurons in striate and extrastriate cortex is profoundly influenced by saccades much smaller than the neurons' receptive fields. In striate cortex (V1) many cells showed a transient decrease in their firing shortly following a saccade. In sharp contrast, cells in the extrastriate areas V2 and V4 showed strong excitatory responses that closely coincided in time with the striate depression. No appreciable activity change was observed in the inferotemporal cortex (IT) following saccades. This activity pattern is consistent with the notion that topographic extrastriate areas receive extraretinal input associated with saccadic events. Such signals may be necessary for the stable perception of objects and scenes during eye movements, mediating the mapping between central object representations and the constantly changing retinotopic input.

Animals

The role of temporal cortical areas in perceptual organization.

The visual areas of the temporal lobe of the primate are thought to be essential for the representation of visual objects. To examine the role of these areas in the visual awareness of a stimulus, we recorded the activity of single neurons in monkeys trained to report their percepts when viewing ambiguous stimuli. Visual ambiguity was induced by presenting incongruent images to the two eyes, a stimulation condition known to instigate binocular rivalry, during which one image is seen at a given time while the other is perceptually suppressed. Previous recordings in areas V1, V2, V4, and MT of monkeys experiencing binocular rivalry showed that only a small proportion of striate and early extrastriate neurons discharge exclusively when the driving stimulus is seen. In contrast, the activity of almost all neurons in the inferior temporal cortex and the visual areas of the cortex of superior temporal sulcus was found to be contingent upon the perceptual dominance of an effective visual stimulus. These areas thus appear to represent a stage of processing beyond the resolution of ambiguities--and thus beyond the processes of perceptual grouping and image segmentation--where neural activity reflects the brain's internal view of objects, rather than the effects of the retinal stimulus on cells encoding simple visual features or shape primitives.

Animals

What is rivalling during binocular rivalry?

When different images are presented to the two eyes, they compete for perceptual dominance, such that one image is visible while the other is suppressed. This binocular rivalry is thought to reflect competition between monocular neurons within the primary visual cortex. However, neurons whose activity correlates with perception during rivalry are found mainly in higher cortical areas, and respond to input from both eyes. Thus rivalry may involve competition between alternative perceptual interpretations at a higher level of analysis. To investigate this, we tested the effect of rapidly alternating the rival stimuli between the two eyes. Under these conditions, the perceptual alternations exhibit the same temporal dynamics as with static patterns, and a single phase of perceptual dominance can span multiple alternations of the stimuli. Thus neural representations of the two stimuli compete for visual awareness independently of the eye through which they reach the higher visual areas. This finding places binocular rivalry in the general category of multistable phenomena, such as ambiguous figures, and provides a new way to study the neural cause and resolution of perceptual ambiguities.

Humans

Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry.

When the two eyes view dissimilar images, we experience binocular rivalry, in which one eye's view dominates for several seconds and is then replaced by that of the other eye. What causes these perceptual changes in the absence of any change in the stimulus? We showed previously that some neurons in monkey cortical area MT show changes in activity during motion rivalry that reflect the perceived direction of motion. To determine whether perception-related modulation of activity occurs in other visual cortical areas, we recorded from individual neurons in V1, V2 and V4 while monkeys reported the perceived orientation of rival gratings of two orthogonal orientations. Many cells, particularly in V4, showed patterns of activity that correlated with the perceptual dominance and suppression of one stimulus. The majority were orientation-selective and could be driven equally well from either eye. It has been previously suggested that binocular rivalry involves reciprocal inhibition between monocular neurons within V1 (for example, see ref. 4), but our results do not support this view; rather, we propose that binocular rivalry arises through interactions between binocular neurons at several levels in the visual pathways, and that similar mechanisms may underlie other multistable perceptual states that occur when viewing ambiguous images.

Animals

Visual object recognition.

Visual object recognition is of fundamental importance to most animals. The diversity of tasks that any biological recognition system must solve suggests that object recognition is not a single, general purpose process. In this review, we consider evidence from the fields of psychology, neuropsychology, and neurophysiology, all of which supports the idea that there are multiple systems for recognition. Data from normal adults, infants, animals, and brain damaged patients reveal a major distinction between the classification of objects at a basic category level and the identification of individual objects from a homogeneous object class. An additional distinction between object representations used for visual perception and those used for visually guided movements provides further support for a multiplicity of visual recognition systems. Recent evidence from psychophysical and neurophysiological studies indicates that one system may represent objects by combinations of multiple views, or aspects, and another may represent objects by structural primitives and their spatial interrelationships.

Adult

Shape representation in the inferior temporal cortex of monkeys.

BACKGROUND: The inferior temporal cortex (IT) of the monkey has long been known to play an essential role in visual object recognition. Damage to this area results in severe deficits in perceptual learning and object recognition, without significantly affecting basic visual capacities. Consistent with these ablation studies is the discovery of IT neurons that respond to complex two-dimensional visual patterns, or objects such as faces or body parts. What is the role of these neurons in object recognition? Is such a complex configurational selectivity specific to biologically meaningful objects, or does it develop as a result of extensive exposure to any objects whose identification relies on subtle shape differences? If so, would IT neurons respond selectively to recently learned views of features of novel objects? The present study addresses this question by using combined psychophysical and electrophysiological experiments, in which monkeys learned to classify and recognize computer-generated three-dimensional objects. RESULTS: A population of IT neurons was found that responded selectively to views of previously unfamiliar objects. The cells discharged maximally to one view of an object, and their response declined gradually as the object was rotated away from this preferred view. No selective responses were ever encountered for views that the animal systematically failed to recognize. Most neurons also exhibited orientation-dependent responses during view-plane rotations. Some neurons were found to be tuned around two views of the same object, and a very small number of cells responded in a view-invariant manner. For the five different objects that were used extensively during the training of the animals, and for which behavioral performance became view-independent, multiple cells were found that were tuned around different views of the same object. A number of view-selective units showed response invariance for changes in the size of the object or the position of its image within the parafovea. CONCLUSION: Our results suggest that IT neurons can develop a complex receptive field organization as a consequence of extensive training in the discrimination and recognition of objects. None of these objects had any prior meaning for the animal, nor did they resemble anything familiar in the monkey's environment. Simple geometric features did not appear to account for the neurons' selective responses. These findings support the idea that a population of neurons--each tuned to a different object aspect, and each showing a certain degree of invariance to image transformations--may, as an ensemble, encode at least some types of complex three-dimensional objects. In such a system, several neurons may be active for any given vantage point, with a single unit acting like a blurred template for a limited neighborhood of a single view.

Animals

View-dependent object recognition by monkeys.

BACKGROUND: How do we recognize visually perceived three-dimensional objects, particularly when they are seen from novel view-points? Recent psychophysical studies have suggested that the human visual system may store a relatively small number of two-dimensional views of a three-dimensional object, recognizing novel views of the object by interpolation between the stored sample views. In order to investigate the neural mechanisms underlying this process, physiological experiments are required and, as a prelude to such experiments, we have been interested to know whether the observations made with human observers extend to monkeys. RESULTS: We trained monkeys to recognize computer-generated images of objects presented from an arbitrarily chosen training view and containing sufficient three-dimensional information to specify the object's structure. We subsequently tested the trained monkeys' ability to generalize recognition of the object to views generated by rotation of the target object around any arbitrary axis. The monkeys recognized as the target only those two-dimensional views that were close to the familiar, training view. Recognition became increasingly difficult for the monkeys as the stimulus was rotated away from the experienced viewpoint, and failed for views farther than about 40 degrees from the training view. This suggests that, in the early stages of learning to recognize a previously unfamiliar object, the monkeys build two-dimensional, viewer-centered object representations, rather than a three-dimensional model of the object. When the animals were trained with as few as three views of the object, 120 degrees apart, they could often recognize all the views of the object resulting from rotations around the same axis. CONCLUSION: Our experiments show that recognition of three-dimensional novel objects is a function of the object's retinal projection. This suggests that non-human primates, like humans, may accomplish view-invariant recognition of familiar objects by a viewer-centered system that interpolates between a small number of stored views. The measures of recognition performance can be simulated by a regularization network that stores a few familiar views, and is endowed with the ability to interpolate between these views. Our results provide the basis for physiological studies of object-recognition by monkeys and suggest that the insights gained from such studies should apply also to humans.

Animals

Parallel pathways in the visual system: their role in perception at isoluminance.

It has been proposed that the functions of the two major parallel channels of the primate visual system, the color-opponent and the broad-band, can be determined in psychophysical experiments by eliminating luminance but maintaining chrominance information (isoluminance), since under such conditions the broad-band channel is believed to be silenced. To test this proposition we examined the visual functions of monkeys after blocking either of these channels and we also assessed the responses of neurons to isoluminant stimuli in the lateral geniculate nucleus. We show that color, texture, stereopsis and pattern perception in the absence of the color-opponent channel, and flicker and motion perception in the absence of the broad-band channel are compromised. Yet isoluminance functions for stereopsis and texture in the absence of the broad-band channel and for motion in the absence of the color-opponent channel are indistinguishable from normal. Our recordings show that the neuronal responses of the broad-band cells for isoluminant exchange of red and green lights are reduced but not eliminated and that the color-opponent cells also become similarly less responsive under these conditions. We conclude that perceptual losses at isoluminance are not specific for either channel.

Animals

Perceptual deficits and the activity of the color-opponent and broad-band pathways at isoluminance.

The deficits in texture, motion, and depth perception incurred in monkeys at isoluminance were compared with the responses of neurons of the color-opponent and broad-band systems in the lateral geniculate nucleus. Texture perception, assumed to be carried by the color-opponent system, and motion and depth perception, ascribed to the broad-band pathway, were all found to be compromised but not abolished at isoluminance. Correspondingly, both the color-opponent and the broad-band systems were affected at isoluminance, but the activity of the neurons in neither system was abolished. These results suggest that impairment of visual capacities at isoluminance cannot be uniquely attributed to either of these systems and that isoluminant stimuli are inappropriate for the psychophysical isolation of these pathways.

Animals

Functions of the colour-opponent and broad-band channels of the visual system.

The colour-opponent and broad-band channels of the primate visual system originate in the retina and remain segregated through several neural stations in the visual system. Until now inferences about their function in vision have been based primarily on studies examining single-cell receptive field properties which have shown that the colour-opponent retinal ganglion cells have small receptive fields, produce sustained responses and receive spatially segregated inputs from different cone types; the broad-band cells have large receptive fields, respond transiently and receive cone inputs that are not spatially separated. We have now examined the visual capacities of rhesus monkeys before and after interrupting either of these channels with small lesions at the lateral geniculate nucleus. Here we report that the colour-opponent channel is essential for the processing of colour, texture, fine pattern and fine stereopsis, whereas the broad-band channel is crucial for the perception of fast flicker and motion. Little or no deficits were found in brightness and coarse-shape discrimination, low spatial frequency stereopsis and contrast sensitivity after the disruption of either of the channels.

Animals

Binocular motion rivalry in macaque monkeys: eye dominance and tracking eye movements.

When the two eyes are exposed to markedly different patterns, perception becomes unstable, falling into oscillations, so that the image of one eye is seen first and then that from the other. With large stimuli the alternation is piecemeal, whilst when small stimuli are used the whole pattern alternates in unison. The purpose of this study was to determine whether a reliable, objective indicator of the perceptual state during binocular rivalry could be developed in the nonhuman primate. Monkeys (Macaca mulatta) were trained to discriminate direction of motion when presented with vertically drifting gratings moving in opposite directions in the two eyes. A high correlation was found between the direction of the slow phase of the optokinetic nystagmus (OKN) elicited by the drifting gratings during rivalry and the direction of motion reported by the monkey even though the gain of the OKN was reduced during rivalry, and the latency was longer. Behavioral eye dominance during rivalry varied significantly over time, between individuals and as a function of interocular contrast differences. Since the direction of tracking eye movements can be used to reliably monitor perceptual state during binocular motion rivalry, the opportunity exists in nonhuman primates to study the neurophysiological mechanisms underlying motion perception during the perceptually ambiguous condition of binocular rivalry.

Animals

The minimum motion technique applied to determine isoluminance in psychophysical experiments with monkeys.

Isoluminance ratios for red/green, red/blue and blue/green sinusoidal gratings were determined in macaque monkeys using the minimum motion heterochromatic photometry technique (Anstis & Cavanagh, 1983), in which the motion of specially constructed test grating reverses at the point of isoluminance. The point of luminance equality between the two colors was determined using (1) overt responses of monkeys trained to discriminate motion direction and (2) reversals in the direction of the nystagmic eye movements. Both measures yielded essentially identical isoluminance points. Both the spatial and the temporal frequency of the grating patterns were found to influence the isoluminance settings in all animals tested. The amount of blue equating a preset red or green value was found to increase consistently with increased spatial frequency and with increasing eccentricity. These results show the necessity of spatial and temporal frequency dependent adjustment of visual patterns used in psychophysical and physiological experiments dealing with the processing of color. Furthermore, eye movement measurements appear to be sufficiently in order to determine isoluminance in foveally presented moving patterns with nonhuman primates.

Animals

The color-opponent and broad-band channels of the primate visual system.

Physiological, anatomical and psychophysical studies have identified several parallel channels of information processing in the primate visual system. Two of these, the color-opponent and the broad-band channels, originate in the retina and remain in part segregated through several higher cortical stations. To improve understanding of their function, recent studies have examined the visual capacities of monkeys following selective disruption of these channels. Color vision, fine- but not coarse-form vision and stereopsis are severely impaired in the absence of the color-opponent channel, whereas motion and flicker perception are impaired at high but not low temporal frequencies in the absence of the broad-band channel. The results suggest that the color-opponent channel extends the range of vision in the spatial and wavelength domains, and that the broad-band channel extends it in the temporal domain. Lesion studies also indicate that these channels must reach higher cortical centers through extrastriate regions other than just area V4 and the middle temporal area, and that the analysis performed by these two regions cannot be uniquely identified with specific visual capacities.

Animals

Role of the color-opponent and broad-band channels in vision.

The functions of the primate color-opponent and broad-band channels were assessed by examining the visual capacities of rhesus monkeys following selective lesions of parvocellular and magnocellular lateral geniculate nucleus, which respectively relay these two channels to the cortex. Parvocellular lesions impaired color vision, high spatial-frequency form vision, and fine stereopsis. Magnocellular lesions impaired high temporal-frequency flicker and motion perception but produced no deficits in stereopsis. Low spatial-frequency form vision, stereopsis, and brightness perception were unaffected by either lesion. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the wavelength and spatial-frequency domains whereas the broad-band channel extends them in the temporal domain.

Animals

Neuronal correlates of subjective visual perception.

Neuronal activity in the superior temporal sulcus of monkeys, a cortical region that plays an important role in analyzing visual motion, was related to the subjective perception of movement during a visual task. Single neurons were recorded while monkeys (Macaca mulatta) discriminated the direction of motion of stimuli that could be seen moving in either of two directions during binocular rivalry. The activity of many neurons was dictated by the retinal stimulus. Other neurons, however, reflected the monkeys' reported perception of motion direction, indicating that these neurons in the superior temporal sulcus may mediate the perceptual experience of a moving object.

Action Potentials

Psychophysical and physiological evidence for viewer-centered object representations in the primate.

A key question concerning the perception of 3D objects is the spatial reference frame used by the brain to represent them. The celerity of the recognition process could be explained by the visual system's ability to quickly transform stored models of familiar 3D objects, or by its ability to specify the relationship among viewpoint-invariant features or volumetric primitives that can be used to accomplish a structural description of an image. Alternatively, viewpoint-invariant recognition could be realized by a system endowed with the ability to perform an interpolation between a set of stored 2D templates, created for each experienced viewpoint. In the present study we set out to examine the nature of object representation in the primate in combined psychophysical-electrophysiological experiments. Monkeys were trained to recognize novel objects from a given viewpoint and subsequently were tested for their ability to generalize recognition for views generated by mathematically rotating the objects around any arbitrary axis. The perception of 3D novel objects was found to be a function of the object's retinal projection at the time of the recognition encounter. Recognition became increasingly difficult for the monkeys as the stimulus was rotated away from its familiar attitude. The generalization field for novel wire-like and spheroidal objects extended to about +/- 40 degrees around an experienced viewpoint. When the animals were trained with as few as three views of the object, 120 degrees apart, they could often interpolate recognition for all views resulting from rotations around the same axis. Recordings from inferotemporal cortex during the psychophysical testing showed a number of neurons with remarkable selectivity for individual views of those objects that the monkey had learned to recognize. Plotting the response of neurons as a function of rotation angle revealed systematic view-tuning curves for rotations in depth. A small percentage of the view-selective cells responded strongly for a particular view and its mirror-symmetrical view. For some of the tested objects, different neurons were found to be tuned to different views of the same object; the peaks of the view-tuning curves were 40-50 degrees apart. Neurons were also found that responded to the sight of unfamiliar objects or distractors. Such cells, however, gave nonspecific responses to a variety of other patterns presented while the monkey performed a simple fixation task.

Animals