Late Visual Areas Research Articles

Perception and memory have distinct spatial tuning properties in human visual cortex

Reactivation of earlier perceptual activity is thought to underlie long-term memory recall. Despite evidence for this view, it is unclear whether mnemonic activity exhibits the same tuning properties as feedforward perceptual activity. Here, we leverage population receptive field models to parameterize fMRI activity in human visual cortex during spatial memory retrieval. Though retinotopic organization is present during both perception and memory, large systematic differences in tuning are also evident. Whereas there is a three-fold decline in spatial precision from early to late visual areas during perception, this pattern is not observed during memory retrieval. This difference cannot be explained by reduced signal-to-noise or poor performance on memory trials. Instead, by simulating top-down activity in a network model of cortex, we demonstrate that this property is well explained by the hierarchical structure of the visual system. Together, modeling and empirical results suggest that computational constraints imposed by visual system architecture limit the fidelity of memory reactivation in sensory cortex.

Neural representations of competing stimuli along the dorsal and ventral visual pathways during binocular rivalry.

Binocular rivalry arises when two discrepant stimuli are simultaneously presented to different eyes, during which observers consciously experience vivid perceptual alternations without physical changes in visual inputs. Neural dynamics tracking such perceptual alternations have been identified at both early and late visual areas, leading to the fundamental debate concerning the primary neural substrate underlying binocular rivalry. One promising hypothesis that might reconcile these seemingly paradoxical findings is a gradual shift from interocular competition between monocular neurons to pattern competition among binocular neurons. Here, we examined this hypothesis by investigating how neural representations of rivalrous stimuli evolved along the visual pathway. We found that representations of the dominant and the suppressed stimuli initially co-existed in V1, which were enhanced and attenuated respectively in extrastriate visual areas. Notably, neural activity in V4 was dictated by the representation of the dominant stimulus, while the representation of the suppressed stimulus was only partially inhibited in dorsal areas V3A and MT+. Our findings revealed a progressive transition from the co-existing representations of the rivalrous inputs to the dictatorial representation of the dominant stimulus in the ventral pathway, and advocated different cortical evolutionary patterns of visual representations between the dorsal and the ventral pathways.

Temporal tuning of repetition suppression across the visual cortex.

The visual system adapts to its recent history. A phenomenon related to this is repetition suppression (RS), a reduction in neural responses to repeated compared with nonrepeated visual input. An intriguing hypothesis is that the timescale over which RS occurs across the visual hierarchy is tuned to the temporal statistics of visual input features, which change rapidly in low-level areas but are more stable in higher level areas. Here, we tested this hypothesis by studying the influence of the temporal lag between successive visual stimuli on RS throughout the visual system using functional (f)MRI. Twelve human volunteers engaged in four fMRI sessions in which we characterized the blood oxygen level-dependent response to pairs of repeated and nonrepeated natural images with interstimulus intervals (ISI) ranging from 50 to 1,000 ms to quantify the temporal tuning of RS along the posterior-anterior axis of the visual system. As expected, RS was maximal for short ISIs and decayed with increasing ISI. Crucially, however, and against our hypothesis, RS decayed at a similar rate in early and late visual areas. This finding challenges the prevailing view that the timescale of RS increases along the posterior-anterior axis of the visual system and suggests that RS is not tuned to temporal input regularities.NEW & NOTEWORTHY Visual areas show reduced neural responses to repeated compared with nonrepeated visual input, a phenomenon termed repetition suppression (RS). Here we show that RS decays at a similar rate in low- and high-level visual areas, suggesting that the short-term decay of RS across the visual hierarchy is not tuned to temporal input regularities. This may limit the specificity with which the mechanisms underlying RS could optimize the processing of input features across the visual hierarchy.

Stimulus- and Neural-Referred Visual Receptive Field Properties following Hemispherectomy: A Case Study Revisited.

Damage to the visual system can result in (a partial) loss of vision, in response to which the visual system may functionally reorganize. Yet the timing, extent, and conditions under which this occurs are not well understood. Hence, studies in individuals with diverse congenital and acquired conditions and using various methods are needed to better understand this. In the present study, we examined the visual system of a young girl who received a hemispherectomy at the age of three and who consequently suffered from hemianopia. We did so by evaluating the corticocortical and retinocortical projections in the visual system of her remaining hemisphere. For the examination of these aspects, we analyzed the characteristics of the connective fields (“neural-referred” receptive fields) based on both resting-state (RS) and retinotopy data. The evaluation of RS data, reflecting brain activity independent from visual stimulation, is of particular interest as it is not biased by the patient's atypical visual percept. We found that, primarily when the patient was at rest, the connective fields between V1 and both early and late visual areas were larger than normal. These abnormally large connective fields could be a sign either of functional reorganization or of unmasked suppressive feedback signals that are normally masked by interhemispheric signals. Furthermore, we confirmed our previous finding of abnormal retinocortical or “stimulus-referred” projections in both early and late visual areas. More specifically, we found an enlarged foveal representation and smaller population receptive fields. These differences could also be a sign of functional reorganization or rather a reflection of the interruption visual information that travels, via the remainder of the visual pathway, from the retina to the visual cortex. To conclude, while we do find indications for relatively subtle changes in visual field map properties, we found no evidence of large-scale reorganization—even though the patient could have benefitted from this. Our work suggests that at a later developmental stage, large-scale reorganization of the visual system no longer occurs, while small-scale properties may still change to facilitate adaptive processing and viewing strategies.

Perceptual size discrimination requires awareness and late visual areas: A continuous flash suppression and interocular transfer study.

We applied continuous flash suppression (CFS) during an interocular transfer paradigm to evaluate the importance of awareness and the contribution of early versus late visual structures in size recognition. Specifically, we tested if size judgements of a visible target could be influenced by a congruent or incongruent prime presented to the same or different eye. Without CFS, participants categorised a target as "small" or "large" more quickly when it was preceded by a congruent prime - regardless of whether the prime and target were presented to the same or different eye. Interocular transfer enabled us to infer that the observed priming was mediated by late visual areas. In contrast, there was no priming under CFS, which underscores the importance of awareness. We conclude that awareness and late visual structures are important for size perception and that any subconscious processing of the stimulus has minimal effect on size recognition.

Perturbation of Posterior Inferior Temporal Cortical Activity Impairs Coarse Orientation Discrimination.

It is reasonable to assume that the discrimination of simple visual stimuli depends on the activity of early visual cortical neurons, because simple visual features are supposedly coded in these areas whereas more complex features are coded in late visual areas. Recently, we showed that training monkeys in a coarse orientation discrimination task modified the response properties of single neurons in the posterior inferior temporal (PIT) cortex, a late visual area. Here, we examined the contribution of PIT to coarse orientation discrimination using causal perturbation methods. Electrical stimulation (ES) of PIT with currents of at least 100 µA impaired coarse orientation discrimination in monkeys. The performance deterioration did not exclusively reflect a general impairment to perform a difficult perceptual task. However, high current (650 µA) but not low-current (100 µA) ES also impaired fine color discrimination. ES of temporal regions dorsal or anterior to PIT produced less impairment of coarse orientation discrimination than ES of PIT. Injections of the GABA agonist muscimol into PIT also impaired performance. These data suggest that the late cortical area PIT is part of the network that supports coarse orientation discrimination of a simple grating stimulus, at least after extensive training in this task at threshold.

The Neural Correlates of Crowding-Induced Changes in Appearance

SummaryObject recognition in the peripheral visual field is limited by crowding: the disruptive influence of nearby clutter [1, 2]. Despite its severity, little is known about the cortical locus of crowding. Here, we examined the neural correlates of crowding by combining event-related fMRI adaptation with a change-detection paradigm [3]. Crowding can change the appearance of objects, such that items become perceptually matched to surrounding objects; we used this change in appearance as a signature of crowding and measured brain activity that correlated with the crowded percept. Observers adapted to a peripheral patch of noise surrounded by four Gabor flankers. When crowded, the noise appears oriented and perceptually indistinguishable from the flankers. Consequently, substitution of the noise for a Gabor identical to the flankers (“change-same”) is rarely detected, whereas substitution for an orthogonal Gabor (“change-different”) is rarely missed. We predicted that brain areas representing the crowded percept would show repetition suppression in change-same trials but release from adaptation in change-different trials. This predicted pattern was observed throughout cortical visual areas V1–V4, increasing in strength from early to late visual areas. These results depict crowding as a multistage process, involving even the earliest cortical visual areas, with perceptual consequences that are increasingly influenced by later visual areas.

The Neural Correlates of Crowding-Induced Changes in Appearance

Summary Object recognition in the peripheral visual field is limited by crowding: the disruptive influence of nearby clutter [1, 2]. Despite its severity, little is known about the cortical locus of crowding. Here, we examined the neural correlates of crowding by combining event-related fMRI adaptation with a change-detection paradigm [3]. Crowding can change the appearance of objects, such that items become perceptually matched to surrounding objects; we used this change in appearance as a signature of crowding and measured brain activity that correlated with the crowded percept. Observers adapted to a peripheral patch of noise surrounded by four Gabor flankers. When crowded, the noise appears oriented and perceptually indistinguishable from the flankers. Consequently, substitution of the noise for a Gabor identical to the flankers (change-same) is rarely detected, whereas substitution for an orthogonal Gabor (change-different) is rarely missed. We predicted that brain areas representing the crowded percept would show repetition suppression in change-same trials but release from adaptation in change-different trials. This predicted pattern was observed throughout cortical visual areas V1–V4, increasing in strength from early to late visual areas. These results depict crowding as a multistage process, involving even the earliest cortical visual areas, with perceptual consequences that are increasingly influenced by later visual areas.

Age differences in neural distinctiveness revealed by multi-voxel pattern analysis

Current theories of cognitive aging argue that neural representations become less distinctive in old age, a phenomenon known as dedifferentiation. The present study used multi-voxel pattern analysis (MVPA) to measure age differences in the distinctiveness of distributed patterns of neural activation evoked by different categories of visual images. We found that neural activation patterns within the ventral visual cortex were less distinctive among older adults. Further, we report that age differences in neural distinctiveness extend beyond the ventral visual cortex: older adults also showed decreased distinctiveness in early visual cortex, inferior parietal cortex, and medial and lateral prefrontal cortex. Neural distinctiveness scores in early and late visual areas were highly correlated, suggesting shared mechanisms of age-related decline. Finally, we investigated whether older adults can compensate for altered processing in visual cortex by encoding stimulus information across larger numbers of voxels within the visual cortex or in regions outside visual cortex. We found no evidence that older adults can increase the distinctiveness of distributed activation patterns, either within or beyond the visual cortex. Our results have important implications for theories of cognitive aging and highlight the value of MVPA to the study of neural coding in the aging brain.

Activity in late visual areas correlates with surface perception

Activity in late visual areas correlates with surface perception

Perceiving electrical stimulation of identified human visual areas

We studied whether detectable percepts could be produced by electrical stimulation of intracranial electrodes placed over human visual areas identified with fMRI. Identification of areas was confirmed by recording local-field potentials from the electrode, such as face-selective electrical responses from electrodes over the fusiform face area (FFA). The probability of detecting electrical stimulation of a visual area varied with the position of the area in the visual cortical hierarchy. Stimulation of early visual areas including V1, V2, and V3 was almost always detected, whereas stimulation of late visual areas such as FFA was rarely detected. When percepts were elicited from late areas, subjects reported that they were simple shapes and colors, similar to the descriptions of percepts from early areas. There were no reports of elaborate percepts, such as faces, even in areas like FFA, where neurons have complex response properties. For sites eliciting percepts, the detection threshold was determined by varying the stimulation current as subjects performed a forced-choice detection task. Current thresholds were similar for late and early areas. The similarity between both percept quality and threshold across early and late areas suggests the presence of functional microcircuits that link electrical stimulation with perception.