Effects of perceptual learning on local stereopsis and neuronal responses of V1 and V2 in prism-reared monkeys

Visual performance improves with practice (perceptual learning). In this study, we sought to determine whether or not adult monkeys reared with early abnormal visual experience improve their stereoacuity by extensive psychophysical training and testing, and if so, whether alterations of neuronal responses in the primary visual cortex (V1) and/or visual area 2 (V2) are involved in such improvement. Strabismus was optically simulated in five macaque monkeys using a prism-rearing procedure between 4 and 14 wk of age. Around 2 yr of age, three of the prism-reared monkeys ("trained" monkeys) were tested for their spatial contrast sensitivity and stereoacuity. Two other prism-reared monkeys received no training or testing ("untrained" monkeys). Microelectrode experiments were conducted around 4 yr of age. All three prism-reared trained monkeys showed improvement in stereoacuity by a factor of 7 or better. However, final stereothresholds were still approximately 10-20 times worse than those in normal monkeys. In V1, disparity sensitivity was drastically reduced in both the trained and untrained prism-reared monkeys and behavioral training had no obvious effect. In V2, the disparity sensitivity in the trained monkeys was better by a factor of approximately 2.0 compared with that in the untrained monkeys. These data suggest that the observed improvement in stereoacuity of the trained prism-reared monkeys may have resulted from better retention of disparity sensitivity in V2 and/or from "learning" by upstream neurons to more efficiently attend to residual local disparity information in V1 and V2.     

Neurophysiological correlates of perceptual learning in the human brain

Summary Rapid learning processes are crucial for human object recognition. We report here on the alterations in neurophysiological activity in the human brain induced by repeated presentation of visual stimuli. In psychophysical experiments the percentage of correct responses increased significantly within less than 30 minutes in untrained observers. This stimulus-specific improvement was not carried over to differently oriented stimuli. Similar learning effects were observed in component latencies of evoked potential field distributions. The occurrence of specific potential field configurations reflected perceptual learning. A spatio-temporal activation pattern with steep gradients over the primary visual cortex appeared to be correlated with plasticity in the human visual system.Supported by the German Research Foundation, DFG Sk 26/5-1, Fa 119/5-2, and Zr 9/1-9. The technical assistance of K. Laschke and B. Tutsch during part of the experiments is gratefully acknowledged.     

Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey

The role of primary visual cortex (V1) in determining the contents of perception is controversial. Human functional magnetic resonance imaging (fMRI) studies of perceptual suppression have revealed a robust drop in V1 activity when a stimulus is subjectively invisible. In contrast, monkey single-unit recordings have failed to demonstrate such perception-locked changes in V1. To investigate the basis of this discrepancy, we measured both the blood oxygen level-dependent (BOLD) response and several electrophysiological signals in two behaving monkeys. We found that all signals were in good agreement during conventional stimulus presentation, showing strong visual modulation to presentation and removal of a stimulus. During perceptual suppression, however, only the BOLD response and the low-frequency local field potential (LFP) power showed decreases, whereas the spiking and high-frequency LFP power were unaffected. These results demonstrate that the coupling between the BOLD and electrophysiological signals in V1 is context dependent, with a marked dissociation occurring during perceptual suppression.     

Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1

Most functional brain imaging studies use task-induced hemodynamic responses to infer underlying changes in neuronal activity. In addition to increases in cerebral blood flow and blood oxygenation level-dependent (BOLD) signals, sustained negative responses are pervasive in functional imaging. The origin of negative responses and their relationship to neural activity remain poorly understood. Through simultaneous functional magnetic resonance imaging and electrophysiological recording, we demonstrate a negative BOLD response (NBR) beyond the stimulated regions of visual cortex, associated with local decreases in neuronal activity below spontaneous activity, detected 7.15 +/- 3.14 mm away from the closest positively responding region in V1. Trial-by-trial amplitude fluctuations revealed tight coupling between the NBR and neuronal activity decreases. The NBR was associated with comparable decreases in local field potentials and multiunit activity. Our findings indicate that a significant component of the NBR originates in neuronal activity decreases.     

Processing of kinetically defined boundaries in areas V1 and V2 of the macaque monkey

We recorded responses in 107 cells in the primary visual area V1 and 113 cells in the extrastriate visual area V2 while presenting a kinetically defined edge or a luminance contrast edge. Cells meeting statistical criteria for responsiveness and orientation selectivity were classified as selective for the orientation of the kinetic edge if the preferred orientation for a kinetic boundary stimulus remained essentially the same even when the directions of the two motion components defining that boundary were changed by 90 degrees. In area V2, 13 of the 113 cells met all three requirements, whereas in V1, only 4 cells met the criteria of 107 that were tested, and even these demonstrated relatively weak selectivity. Correlation analysis showed that V1 and V2 populations differed greatly (P < 1.0 x 10(-6), Student's t-test) in their selectively for specific orientations of kinetic edge stimuli. Neurons in V2 that were selective for the orientation of a kinetic boundary were further distinguished from their counterparts in V1 in displaying a strong, sharply tuned response to a luminance edge of the same orientation. We concluded that selectivity for the orientation of kinetically defined boundaries first emerges in area V2 rather than in primary visual cortex. An analysis of response onset latencies in V2 revealed that cells selective for the orientation of the motion-defined boundary responded about 40 ms more slowly, on average, to the kinetic edge stimulus than to a luminance edge. In nonselective cells, that is, those presumably responding only to the local motion in the stimulus, this difference was only about 20 ms. Response latencies for the luminance edge were indistinguishable in KE-selective and -nonselective neurons. We infer that while responses to luminance edges or local motion are indigenous to V2, KE-selective responses may involve feedback entering the ventral stream at a point downstream with respect to V2.     

Human perceptual learning in the peripheral visual field: sensory thresholds and neurophysiological correlates

Perceptual learning in the peripheral visual field was studied in 24 adults using vernier targets. The aim was to relate perceptual improvements to changes of electrical brain activity. Thresholds were measured before, during, and after training, and on the next day. During training, the subjects passively looked at suprathreshold targets, and EEG activity was recorded from 30 electrodes over the occipital brain areas. Mean evoked potentials were computed for the first and second block of 1200 stimulus presentations, and the scalp topography of visual evoked potential (VEP) activity was analysed. Only for the stimulated area, training resulted initially in increased thresholds that, however, decreased significantly after consolidation. Electrical brain activity displayed smaller field strength and altered topography after training. Some of the effects were caused by habituation or adaptation to the training stimuli resulting in less efficient neurophysiological processing. The topographical changes indicate that different neuronal elements were activated after perceptual learning.     

Cross-correlation study of the temporal interactions between areas V1 and V2 of the macaque monkey

Cross-correlation studies performed in cat visual cortex have shown that neurons in different cortical areas of the same hemisphere or in corresponding areas of opposite hemispheres tend to synchronize their activities. The presence of synchronization may be related to the parallel organization of the cat visual system, in which different cortical areas can be activated in parallel from the lateral geniculate nucleus. We wanted to determine whether interareal synchronization of firing can also be observed in the monkey, in which cortical areas are thought to be organized in a hierarchy spanning different levels. Cross-correlation histograms (CCHs) were calculated from pairs of single or pairs of multiunit activities simultaneously recorded in areas V1 and V2 of paralyzed and anesthetized macaque monkeys. Moving bars and flashed bars were used as stimuli. The shift predictor was calculated and subtracted from the raw CCH to reveal interactions of neuronal origin in isolation. Significant CCH peaks, indicating interactions of neuronal origin, were obtained in 11% of the dual single-unit recordings and 46% of the dual multiunit recordings with moving bars. The incidence of nonflat CCHs with flashed bars was 29 and 78%, respectively. For the pairs of recording sites where both flashed and moving stimuli were used, the incidences of significant CCHs were very similar. Three types of peaks were distinguished on the basis of their width at half-height: T (<16 ms), C (between 16 and 180 ms), and H peaks (>180 ms). T peaks were very rarely observed (<1% in single-unit recordings). H peaks were observed in 7-16% of the single-unit CCHs, and C peaks in 6-16%, depending on the stimulus used. C and H peaks were observed more often when the receptive fields were overlapping or distant by <2 degrees. To test for the presence of synchronization between neurons in areas V1 and V2, we measured the position of the CCH peak with respect to the origin of the time axis of the CCH. Only in the case of a few T peaks did we find displaced peaks, indicating a possible drive of the V2 neuron by the simultaneously recorded V1 cell. All the other peaks were either centered on the origin or overlapped the origin of time with their upper halves. Thus similarly to what has been reported for the cat, neurons belonging to different cortical areas in the monkey tend to synchronize the time of emission of their action potentials with three different levels of temporal precision. For peaks calculated from flashed stimuli, we compared the peak position with the difference between latencies of V1 and V2 neurons. There was a clear correlation for single-unit pairs in the case of C peaks. Thus the position of a C peak on the time axis appears to reflect the order of visual activation of the correlated neurons. The coupling strength for H peaks was smaller during visual drive compared with spontaneous activity. On the contrary, C peaks were seen more often and were stronger during visual stimulation than during spontaneous activity. This suggests that C-type synchronization is associated with the processing of visual information. The origin of synchronized activity in a serially organized system is discussed.     

Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: influence of eccentricity

One hundred and forty two neurons in V1 and V2 were quantitatively tested using a multihistogram technique in paralyzed and anesthetized macaque monkeys. V1 neurons with receptive fields within 2 degrees from the fixation point (central V1 sample) and V1 neurons with eccentric receptive fields (15-25 degrees eccentricity, peripheral V1 sample) were compared to assess changes in velocity sensitivity and direction selectivity with eccentricity. The central V1 sample was compared with V2 neurons with receptive fields in the same part of the visual field (central V2 sample) to compare the involvement of both areas in the analysis of motion. Velocity sensitivity of V1 neurons shifts to faster velocities with increasing eccentricity. V1 and V2 neurons subserving central vision have similar preference for slow movements. All neurons could be classified into three categories according to their velocity-response curves: velocity low pass, velocity broad band, and velocity tuned. Most cells in parts of V1 and V2 subserving central vision are velocity low pass. As eccentricity increases in V1, velocity low-pass cells give way to velocity broad-band cells. There is a significant correlation between velocity upper cutoff and receptive field width among V1 neurons. The change in upper cutoff velocity with eccentricity depends both on temporal and spatial factors. Direction selectivity depends on stimulus velocity in most V1 cells. Neurons in the central V1 sample retain their direction selectivity at lower speeds than do neurons in the peripheral V1 sample. The proportion of direction-selective cells is low in both V1 and V2. In V1, direction selectivity decreases with eccentricity. In V1, both velocity upper cutoff and direction selectivity correlate more with laminar position than with receptive field type. The similarity between V1 of the monkey and area 17 of the cat, and the dissimilarity between V2 of the monkey and area 18 of the cat, are discussed.     

Dynamics of response to perceptual pop-out stimuli in macaque V1

Contextual modulation due to feature contrast between the receptive field and surrounding region has been reported for numerous stimuli in primary visual cortex. One type of this modulation, iso-orientation surround suppression, has been studied extensively. The degree to which surround suppression is related to other forms of contextual modulation remains unknown. We used shape-from-shading stimuli in a field of distractors to test the latency and magnitude of contextual modulation to a stimulus that cannot be distinguished with an orientation-selective mechanism. This stimulus configuration readily elicits perceptual pop-out in human observers and induces a long-latency contextual modulation response in neurons in macaque early visual cortex. We found that animals trained to detect the location of a pop-out stimulus were better at finding a sphere that appeared to be lit from below in the presence of distractors that were lit from above. Furthermore, neuronal responses were stronger and had shorter latency in the condition where behavioral performance was best. This asymmetry is compatible with earlier psychophysical findings in human observers. In the population of V1 neurons, the latency of the contextual modulation response is 145 ms on average (ranging from 70 to 230 ms). This is much longer than the latency for iso-orientation surround suppression, indicating that the underlying circuitry is distinct. Our results support the idea that a feature-specific feedback signal generates the pop-out responses we observe and suggest that V1 neurons actively participate in the computation of perceptual salience.     

Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities

It is often assumed that the action of cortical feedback connections is slow and modulatory, whereas feedforward connections carry a rapid drive to their target neurons. Recent results from our laboratory showed a very rapid effect of feedback connections on the visual responses of neurons in lower order areas. We wanted to determine whether such a rapid action is mediated by fast conducting axons. Using electrical stimulation, we compared the conduction velocities along feedforward and feedback axons between areas V1 and V2 of the macaque monkey. We conclude that feedback and feedforward connections between V1 and V2 have comparable fast conduction velocities (around 3.5 m/s).     

Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area

This study aimed to identify neural mechanisms that underlie perceptual learning in a visual-discrimination task. We trained two monkeys (Macaca mulatta) to determine the direction of visual motion while we recorded from their middle temporal area (MT), which in trained monkeys represents motion information that is used to solve the task, and lateral intraparietal area (LIP), which represents the transformation of motion information into a saccadic choice. During training, improved behavioral sensitivity to weak motion signals was accompanied by changes in motion-driven responses of neurons in LIP, but not in MT. The time course and magnitude of the changes in LIP correlated with the changes in behavioral sensitivity throughout training. Thus, for this task, perceptual learning does not appear to involve improvements in how sensory information is represented in the brain, but rather how the sensory representation is interpreted to form the decision that guides behavior.     

Early and rapid perceptual learning

Major, rapid performance improvements in perceptual training are often dismissed as 'task' or 'procedural' learning because they are fast and generalize within a task. We assessed the contributions of perceptual and procedural learning to improvement in an auditory tone frequency learning task in humans and found that perceptual learning accounted for between 76% and 98% of the rapid early performance improvement.     

Electrophysiological correlates of visual perceptual masking in monkeys

Summary Monkeys were trained to discriminate with nearly 100% accuracy between a square and a triangle presented simultaneously in a brief tachistoscopic flash. Perceptual masking was demonstrated by inability to perform this trained visual discrimination at better than chance level when the information flash was followed in less than 20 msec by a blank second flash. In order to determine the nature and locus of this retroactive visual perceptual masking effect, electrical potentials were recorded simultaneously from three points along the optic pathways: optic nerve or tract, lateral geniculate body, and visual cortex. Potentials were computer-averaged and correlated with the monkey's ability or inability to make a correct behavioral response to the information contained in the first or test flash (T). When the perception of T was masked by the second or blanking flash (B), only the evoked potential characteristic of B was observed at all recording sites, including the optic nerve or tract. This suggested that the interaction underlying masking occurred in the retina since optic nerve or tract responses are dependent upon retinal ganglion cells. When T was not masked, an early portion of the evoked response to T could be detected at all recording sites. Perception of T was possible when only the initial segment of the T-potential (15 msec or less) was present at each recording site. Thus the visual information transfer essential to the performance of an already learned visual discrimination task appears to occur very early in the course of the evoked response and is not dependent upon later or secondary components.Supported by grants from the Office of Naval Research (Nonr-4756) and National Aeronautics and Space Administration (NASA NGL 05-007-049). Aided by National Institute of Mental Health Training Grant 5 TI MH-6415.     

Temporal properties of inputs to direction-selective neurons in monkey V1

Motion in the visual scene is processed by direction-selective neurons in primary visual cortex. These cells receive inputs that differ in space and time. What are these inputs? A previous single-unit recording study in anesthetized monkey V1 proposed that the two major streams arising in the primate retina, the M and P pathways, differed in space and time as required to create direction selectivity. We confirmed that cortical cells driven by P inputs tend to have sustained responses. The M pathway, however, as assessed by recordings in layer 4Calpha and from cells with high contrast sensitivity, is not purely transient. The diversity of timing in the M stream suggests that combinations of M inputs, as well as of M and P inputs, create direction selectivity.     

Neurons in monkey visual area V2 encode combinations of orientations

Contours and textures are important attributes of object surfaces, and are often described by combinations of local orientations in visual images. To elucidate the neural mechanisms underlying contour and texture processing, we examined receptive field (RF) structures of neurons in visual area V2 of the macaque monkey for encoding combinations of orientations. By measuring orientation tuning at several locations within the classical RF, we found that a majority (70%) of V2 neurons have similar orientation tuning throughout the RF. However, many others have RFs containing subregions tuned to different orientations, most commonly about 90 degrees apart. By measuring interactions between two positions within the RF, we found that approximately one-third of neurons show inhibitory interactions that make them selective for combinations of orientations. These results indicate that V2 neurons could play an important role in analyzing contours and textures and could provide useful cues for surface segmentation.     

Neural coding of spatial phase in V1 of the macaque monkey

We examine the responses of single neurons and pairs of neurons, simultaneously recorded with a single tetrode in the primary visual cortex of the anesthetized macaque monkey, to transient presentations of stationary gratings of varying spatial phase. Such simultaneously recorded neurons tended to have similar tuning to the phase of the grating. To determine the response features that reliably discriminate these stimuli, we use the metric-space approach extended to pairs of neurons. We find that paying attention to the times of individual spikes, at a resolution of approximately 30 ms, and keeping track of which neuron fires which spike rather than just the summed local activity contribute substantially to phase coding. The contribution is both quantitative (increasing the fidelity of phase coding) and qualitative (enabling a 2-dimensional "response space" that corresponds to the spatial phase cycle). We use a novel approach, the extraction of "temporal profiles" from the metric space analysis, to interpret and compare temporal coding across neurons. Temporal profiles were remarkably consistent across a large subset of neurons. This consistency indicates that simple mechanisms (e.g., comparing the size of the transient and sustained components of the response) allow the temporal contribution to phase coding to be decoded.     

Visual activity in areas V3a and V3 during reversible inactivation of area V1 in the macaque monkey.

1. Behavioral studies in the monkey and clinical studies in humans show that some visuomotor functions are spared in case of a V1 lesion. This residual vision appears to be subserved at least partially by visual activity in extrastriate cortex. Earlier studies have demonstrated that neurons in area V2 lose their visual responses when V1 is reversibly inactivated. On the other hand, Rodman and collaborators have recently shown that neurons in the middle temporal area (area MT) remain visually responsive when V1 is lesioned or inactivated. The purpose of the present study was to determine whether area MT is unique among extrastriate cortical areas in containing visually responsive neurons in the absence of input from area 17. 2. A circular part of the opercular region of area V1 was reversibly inactivated by cooling with a Peltier device. In that condition, 149 sites were recorded in the retinotopically corresponding regions of areas V3 and V3a. 3. About 30% of sites in area V3a still responded to visual stimulation when V1 was inactivated. On the contrary, nearly all sites in area V3 ceased to fire to visual stimulation. Receptive-field properties were assessed with qualitative measures; for most single cells or multiunit sites that responded during V1 inactivation, these properties did not change during cooling. 4. These results suggest that area V3a could take part in spared visuomotor abilities in case of a lesion of V1. Areas V3a and MT are both part of the occipitoparietal pathway, which suggests that the residual vision observed after a lesion of area 17 may depend mostly on this pathway.     

Neural correlates of evidence accumulation in a perceptual decision task

Sequential sampling models provide a useful framework for understanding human decision making. A key component of these models is an evidence accumulation process in which information is accrued over time to a threshold, at which point a choice is made. Previous neurophysiological studies on perceptual decision making have suggested accumulation occurs only in sensorimotor areas involved in making the action for the choice. Here we investigated the neural correlates of evidence accumulation in the human brain using functional magnetic resonance imaging (fMRI) while manipulating the quality of sensory evidence, the response modality, and the foreknowledge of the response modality. We trained subjects to perform a random dot motion direction discrimination task by either moving their eyes or pressing buttons to make their responses. In addition, they were cued about the response modality either in advance of the stimulus or after a delay. We isolated fMRI responses for perceptual decisions in both independently defined sensorimotor areas and task-defined nonsensorimotor areas. We found neural signatures of evidence accumulation, a higher fMRI response on low coherence trials than high coherence trials, primarily in saccade-related sensorimotor areas (frontal eye field and intraparietal sulcus) and nonsensorimotor areas in anterior insula and inferior frontal sulcus. Critically, such neural signatures did not depend on response modality or foreknowledge. These results help establish human brain areas involved in evidence accumulation and suggest that the neural mechanism for evidence accumulation is not specific to effectors. Instead, the neural system might accumulate evidence for particular stimulus features relevant to a perceptual task.