The representation of the ipsilateral visual field in human cerebral cortex

Previous studies of cortical retinotopy focused on influences from the contralateral visual field, because ascending inputs to cortex are known to be crossed. Here, functional magnetic resonance imaging was used to demonstrate and analyze an ipsilateral representation in human visual cortex. Moving stimuli, in a range of ipsilateral visual field locations, revealed activity: (i) along the vertical meridian in retinotopic (presumably lower-tier) areas; and (ii) in two large branches anterior to that, in presumptive higher-tier areas. One branch shares the anterior vertical meridian representation in human V3A, extending superiorly toward parietal cortex. The second branch runs antero-posteriorly along lateral visual cortex, overlying motion-selective area MT. Ipsilateral stimuli sparing the region around the vertical meridian representation also produced signal reductions (perhaps reflecting neural inhibition) in areas showing contralaterally driven retinotopy. Systematic sampling across a range of ipsilateral visual field extents revealed significant increases in ipsilateral activation in V3A and V4v, compared with immediately posterior areas V3 and VP. Finally, comparisons between ipsilateral stimuli of different types but equal retinotopic extent showed clear stimulus specificity, consistent with earlier suggestions of a functional segregation of motion vs. form processing in parietal vs. temporal cortex, respectively.

Shift in speed selectivity of visual cortical neurons: A neural basis of perceived motion contrast

The perceived speed of motion in one part of the visual field is influenced by the speed of motion in its surrounding fields. Little is known about the cellular mechanisms causing this phenomenon. Recordings from mammalian visual cortex revealed that speed preference of the cortical cells could be changed by displaying a contrast speed in the field surrounding the cell’s classical receptive field. The neuron’s selectivity shifted to prefer faster speed if the contextual surround motion was set at a relatively lower speed, and vice versa. These specific center–surround interactions may underlie the perceptual enhancement of speed contrast between adjacent fields.

Excitatory–inhibitory network in the visual cortex: Psychophysical evidence

At early stages in visual processing cells respond to local stimuli with specific features such as orientation and spatial frequency. Although the receptive fields of these cells have been thought to be local and independent, recent physiological and psychophysical evidence has accumulated, indicating that the cells participate in a rich network of local connections. Thus, these local processing units can integrate information over much larger parts of the visual field; the pattern of their response to a stimulus apparently depends on the context presented. To explore the pattern of lateral interactions in human visual cortex under different context conditions we used a novel chain lateral masking detection paradigm, in which human observers performed a detection task in the presence of different length chains of high-contrast-flanked Gabor signals. The results indicated a nonmonotonic relation of the detection threshold with the number of flankers. Remote flankers had a stronger effect on target detection when the space between them was filled with other flankers, indicating that the detection threshold is caused by dynamics of large neuronal populations in the neocortex, with a major interplay between excitation and inhibition. We considered a model of the primary visual cortex as a network consisting of excitatory and inhibitory cell populations, with both short- and long-range interactions. The model exhibited a behavior similar to the experimental results throughout a range of parameters. Experimental and modeling results indicated that long-range connections play an important role in visual perception, possibly mediating the effects of context.

Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations

Gamma frequency (about 20–70 Hz) oscillations occur during novel sensory stimulation, with tight synchrony over distances of at least 7 mm. Synchronization in the visual system has been proposed to reflect coactivation of different parts of the visual field by a single spatially extended object. We have shown that intracortical mechanisms, including spike doublet firing by interneurons, can account for tight long-range synchrony. Here we show that synchronous gamma oscillations in two sites also can cause long-lasting (>1 hr) potentiation of recurrent excitatory synapses. Synchronous oscillations lasting >400 ms in hippocampal area CA1 are associated with an increase in both excitatory postsynaptic potential (EPSP) amplitude and action potential afterhyperpolarization size. The resulting EPSPs stabilize and synchronize a prolonged beta frequency (about 10–25 Hz) oscillation. The changes in EPSP size are not expressed during non-oscillatory behavior but reappear during subsequent gamma-oscillatory events. We propose that oscillation-induced EPSPs serve as a substrate for memory, whose expression either enhances or blocks synchronization of spatially separated sites. This phenomenon thus provides a dynamical mechanism for storage and retrieval of stimulus-specific neuronal assemblies.

Covert attention accelerates the rate of visual information processing

Whenever we open our eyes, we are confronted with an overwhelming amount of visual information. Covert attention allows us to select visual information at a cued location, without eye movements, and to grant such information priority in processing. Covert attention can be voluntarily allocated, to a given location according to goals, or involuntarily allocated, in a reflexive manner, to a cue that appears suddenly in the visual field. Covert attention improves discriminability in a wide variety of visual tasks. An important unresolved issue is whether covert attention can also speed the rate at which information is processed. To address this issue, it is necessary to obtain conjoint measures of the effects of covert attention on discriminability and rate of information processing. We used the response-signal speed-accuracy tradeoff (SAT) procedure to derive measures of how cueing a target location affects speed and accuracy in a visual search task. Here, we show that covert attention not only improves discriminability but also accelerates the rate of information processing.

Neural mechanisms for visual memory and their role in attention

Recent studies show that neuronal mechanisms for learning and memory both dynamically modulate and permanently alter the representations of visual stimuli in the adult monkey cortex. Three commonly observed neuronal effects in memory-demanding tasks are repetition suppression, enhancement, and delay activity. In repetition suppression, repeated experience with the same visual stimulus leads to both short- and long-term suppression of neuronal responses in subpopulations of visual neurons. Enhancement works in an opposite fashion, in that neuronal responses are enhanced for objects with learned behavioral relevance. Delay activity is found in tasks in which animals are required to actively hold specific information “on-line” for short periods. Repetition suppression appears to be an intrinsic property of visual cortical areas such as inferior temporal cortex and is thought to be important for perceptual learning and priming. By contrast, enhancement and delay activity may depend on feedback to temporal cortex from prefrontal cortex and are thought to be important for working memory. All of these mnemonic effects on neuronal responses bias the competitive interactions that take place between stimulus representations in the cortex when there is more than one stimulus in the visual field. As a result, memory will often determine the winner of these competitions and, thus, will determine which stimulus is attended.

Lightness constancy in primary visual cortex

When the illumination of a visual scene changes, the quantity of light reflected from objects is altered. Despite this, the perceived lightness of the objects generally remains constant. This perceptual lightness constancy is thought to be important behaviorally for object recognition. Here we show that interactions from outside the classical receptive fields of neurons in primary visual cortex modulate neural responses in a way that makes them immune to changes in illumination, as is perception. This finding is consistent with the hypothesis that the responses of neurons in primary visual cortex carry information about surface lightness in addition to information about form. It also suggests that lightness constancy, which is sometimes thought to involve “higher-level” processes, is manifest at the first stage of visual cortical processing.

Selective attention to stimulus location modulates the steady-state visual evoked potential.

Steady-state visual evoked potentials (SSVEPs) were recorded from the scalp of human subjects who were cued to attend to a rapid sequence of alphanumeric characters presented to one visual half-field while ignoring a concurrent sequence of characters in the opposite half-field. These two-character sequences were each superimposed upon a small square background that was flickered at a rate of 8.6 Hz in one half-field and 12 Hz in the other half-field. The amplitude of the frequency-coded SSVEP elicited by either of the task-irrelevant flickering backgrounds was significantly enlarged when attention was focused upon the character sequence at the same location. This amplitude enhancement with attention was most prominent over occipital-temporal scalp areas of the right cerebral hemisphere regardless of the visual field of stimulation. These findings indicate that the SSVEP reflects an enhancement of neural responses to all stimuli that fall within the "spotlight" of spatial attention, whether or not the stimuli are task-relevant. Recordings of the SSVEP provide a new approach for studying the neural mechanisms and functional properties of selective attention to multi-element visual displays.

Mapping striate and extrastriate visual areas in human cerebral cortex.

Functional magnetic resonance imaging (fMRI) was used to identify and map the representation of the visual field in seven areas of human cerebral cortex and to identify at least two additional visually responsive regions. The cortical locations of neurons responding to stimulation along the vertical or horizontal visual field meridia were charted on three-dimensional models of the cortex and on unfolded maps of the cortical surface. These maps were used to identify the borders among areas that would be topographically homologous to areas V1, V2, V3, VP, and parts of V3A and V4 of the macaque monkey. Visually responsive areas homologous to the middle temporal/medial superior temporal area complex and unidentified parietal visual areas were also observed. The topography of the visual areas identified thus far is consistent with the organization in macaque monkeys. However, these and other findings suggest that human and simian cortical organization may begin to differ in extrastriate cortex at, or beyond, V3A and V4.

Numerical representations in primates.

Research has demonstrated that human infants and nonhuman primates have a rudimentary numerical system that enables them to count objects or events. More recently, however, studies using a preferential looking paradigm have suggested that preverbal human infants are capable of simple arithmetical operations, such as adding and subtracting a small number of visually presented objects. These findings implicate a relatively sophisticated representational system in the absence of language. To explore the evolutionary origins of this capacity, we present data from an experiment with wild rhesus monkeys (Macaca mulatta) that methodologically mirrors those conducted on human infants. Results suggest that rhesus monkeys detect additive and subtractive changes in the number of objects present in their visual field. Given the methodological and empirical similarities, it appears that nonhuman primates such as rhesus monkeys may also have access to arithmetical representations, although alternative explanations must be considered for both primate species.

Spatial integration and cortical dynamics.

Cells in adult primary visual cortex are capable of integrating information over much larger portions of the visual field than was originally thought. Moreover, their receptive field properties can be altered by the context within which local features are presented and by changes in visual experience. The substrate for both spatial integration and cortical plasticity is likely to be found in a plexus of long-range horizontal connections, formed by cortical pyramidal cells, which link cells within each cortical area over distances of 6-8 mm. The relationship between horizontal connections and cortical functional architecture suggests a role in visual segmentation and spatial integration. The distribution of lateral interactions within striate cortex was visualized with optical recording, and their functional consequences were explored by using comparable stimuli in human psychophysical experiments and in recordings from alert monkeys. They may represent the substrate for perceptual phenomena such as illusory contours, surface fill-in, and contour saliency. The dynamic nature of receptive field properties and cortical architecture has been seen over time scales ranging from seconds to months. One can induce a remapping of the topography of visual cortex by making focal binocular retinal lesions. Shorter-term plasticity of cortical receptive fields was observed following brief periods of visual stimulation. The mechanisms involved entailed, for the short-term changes, altering the effectiveness of existing cortical connections, and for the long-term changes, sprouting of axon collaterals and synaptogenesis. The mutability of cortical function implies a continual process of calibration and normalization of the perception of visual attributes that is dependent on sensory experience throughout adulthood and might further represent the mechanism of perceptual learning.

Localization of visual stimuli after striate cortex damage in monkeys: parallels with human blindsight.

Blindsight is a phenomenon in which human patients with damage to striate cortex deny any visual sensation in the resultant visual field defect but can nonetheless detect and localize stimuli when persuaded to guess. Although monkeys with striate lesions have also been shown to exhibit some residual vision, it is not yet clear to what extent the residual capacities in monkeys parallel the phenomenon of human blindsight. To clarify this issue, we trained two monkeys with unilateral lesions of striate cortex to make saccadic eye movements to visual targets in both hemifields under two conditions. In the condition analogous to clinical perimetry, they failed to initiate saccades to targets presented in the contralateral hemifield and thus appeared "blind." Only in the condition where the fixation point was turned off simultaneously with the onset of the target--signaling the animal to respond at the appropriate time--were monkeys able to localize targets contralateral to the striate lesion. These results indicate that the conditions under which residual vision is demonstrable are similar for monkeys with striate cortex damage and humans with blindsight.

Binocular vision in insects: How mantids solve the correspondence problem

Praying mantids use binocular cues to judge whether their prey is in striking distance. When there are several moving targets within their binocular visual field, mantids need to solve the correspondence problem. They must select between the possible pairings of retinal images in the two eyes so that they can strike at a single real target. In this study, mantids were presented with two targets in various configurations, and the resulting fixating saccades that precede the strike were analyzed. The distributions of saccades show that mantids consistently prefer one out of several possible matches. Selection is in part guided by the position and the spatiotemporal features of the target image in each eye. Selection also depends upon the binocular disparity of the images, suggesting that insects can perform local binocular computations. The pairing rules ensure that mantids tend to aim at real targets and not at “ghost” targets arising from false matches.

Role of intrinsic synaptic circuitry in collicular sensorimotor integration

The superficial gray layer of the superior colliculus contains a map that represents the visual field, whereas the underlying intermediate gray layer contains a vector map of the saccades that shift the direction of gaze. These two maps are aligned so that a particular region of the visual field is represented directly above the neurons that orient the highest acuity area of the retina toward that region. Although it has been proposed that the transmission of information from the visuosensory to the motor map plays an important role in the generation of visually guided saccades, experiments have failed to demonstrate any functional linkage between the two layers. We examined synaptic transmission between these layers in vitro by stimulating the superficial layer while using whole-cell patch-clamp methods to measure the responses of intermediate layer neurons. Stimulation of superficial layer neurons evoked excitatory postsynaptic currents in premotor cells. This synaptic input was columnar in organization, indicating that the connections between the layers link corresponding regions of the visuosensory and motor maps. Excitatory postsynaptic currents were large enough to evoke action potentials and often occurred in clusters similar in duration to the bursts of action potentials that premotor cells use to command saccades. Our results indicate the presence of functional connections between the superficial and intermediate layers and show that such connections could play a significant role in the generation of visually guided saccades.