Modulation of sensory suppression: implications for receptive field sizes in the human visual cortex

Neurophysiological studies in monkeys show that when multiple visual stimuli appear simultaneously in the visual field, they are not processed independently, but rather interact in a mutually suppressive way. This suggests that multiple stimuli compete for neural representation. Consistent with this notion, we have previously found in humans that functional magnetic resonance imaging (fMRI) signals in V1 and ventral extrastriate areas V2, V4, and TEO are smaller for simultaneously presented (i.e., competing) stimuli than for the same stimuli presented sequentially (i.e., not competing). Here we report that suppressive interactions between stimuli are also present in dorsal extrastriate areas V3A and MT, and we compare these interactions to those in areas V1 through TEO. To exclude the possibility that the differences in responses to simultaneously and sequentially presented stimuli were due to differences in the number of transient onsets, we tested for suppressive interactions in area V4, in an experiment that held constant the number of transient onsets. We found that the fMRI response to a stimulus in the upper visual field was suppressed by the presence of nearby stimuli in the lower visual field. Further, we excluded the possibility that the greater fMRI responses to sequential compared with simultaneous presentations were due to exogeneous attentional cueing by having our subjects count T's or L's at fixation, an attentionally demanding task. Behavioral testing demonstrated that neither condition interfered with performance of the T/L task. Our previous findings suggested that suppressive interactions among nearby stimuli in areas V1 through TEO were scaled to the receptive field (RF) sizes of neurons in those areas. Here we tested this idea by parametrically varying the spatial separation among stimuli in the display. Display sizes ranged from 2 x 2 degrees to 7 x 7 degrees and were centered at 5.5 degrees eccentricity. Based on the effects of display size on the magnitude of suppressive interactions, we estimated that RF sizes at an eccentricity of 5.5 degrees were <2 degrees in V1, 2-4 degrees in V2, 4-6 degrees in V4, larger than 7 degrees (but still confined to a quadrant) in TEO, and larger than 6 degrees (confined to a quadrant) in V3A. These estimates of RF sizes in human visual cortex are strikingly similar to those measured in physiological mapping studies in the homologous visual areas in monkeys.     

Electrophysiological correlates of human intrasaccadic processing

Visual discrimination performance is thought to be suppressed during saccades in order to contribute to space constancy. However, under certain experimental conditions, visual inhibition may not take place, suggesting a more complex underlying mechanism. We tested the discrimination ability of 20 healthy subjects during visually guided horizontal saccades and recorded simultaneously the evoked brain activity from 30 channels over occipital, parietal, and temporal areas. During the execution of saccadic eye movements, visual stimuli were presented for 30 ms. In order to prevent retinal afterimages, stimuli were followed by a visual mask. In a control condition, the same stimuli were presented with stationary eyes. Electro-oculogram (EOG) and electroencephalogram (EEG) signals were recorded continuously together with information about the stimuli and the subject's response. Evoked potentials were computed offline, and component latency, field strength (global field power), and topography were compared between conditions. During saccades, subjects showed only slightly reduced discrimination performance which remained very high above the chance level; thus, there was no evidence for strong saccadic suppression with the supra-threshold stimuli employed. However, the cortical activation patterns exhibited large alteration when a physically identical stimulus was presented during the eye movement: around 130 ms latency, field strength was significantly smaller than when stationary targets were processed, and scalp topography was also different. These effects on evoked field distributions may be attributed to neural interactions of an efference copy signal (linked to the oculomotor command) with the afferent excitation following the visual stimulus.     

The speed of context integration in the visual cortex

The observation of figure-ground selectivity in neurons of the visual cortex shows that these neurons can be influenced by the image context far beyond the classical receptive field. To clarify the nature of the context integration mechanism, we studied the latencies of neural edge signals, comparing the emergence of context-dependent definition of border ownership with the onset of local edge definition (contrast polarity; stereoscopic depth order). Single-neuron activity was recorded in areas V1 and V2 of Macaca mulatta under behaviorally induced fixation. Whereas local edge definition emerged immediately (<13 ms) after the edge onset response, the context-dependent signal was delayed by about 30 ms. To see if the context influence was mediated by horizontal fibers within cortex, we measured the latencies of border ownership signals for two conditions in which the relevant context information was located at different distances from the receptive field and compared the latency difference with the difference predicted from horizontal signal propagation. The prediction was based on the increase in cortical distance, computed from the mapping of the test stimuli in the cortex, and the known conduction velocities of horizontal fibers. The measured latencies increased with cortical distance, but much less than predicted by the horizontal propagation hypothesis. Probability calculations showed that an explanation of the context influence by horizontal signal propagation alone is highly unlikely, whereas mechanisms involving back projections from other extrastriate areas are plausible.     

SMI-32 parcellates the visual cortical areas of the marmoset

The distribution pattern of SMI-32-immunoreactivity (SMI-32-ir) of neuronal elements was examined in the visual cortical areas of marmoset monkey. Layer IV of the primary visual cortex (V1) and layers III and V of the extrastriate areas showed the most abundant SMI-32-ir. The different areal and laminar distribution of SMI-32-ir allowed the distinction between various extrastriate areas and determined their exact anatomical boundaries in the New World monkey, Callithrix penicillata. It is shown here that the parcellating nature of SMI-32 described earlier in the visual cortical areas of other mammals - including Old World monkeys - is also present in the marmoset. Furthermore, a comparison became possible between the chemoanatomical organization of New World and Old World primates' visual cortical areas.     

Sources of attention-sensitive visual event-related potentials

Summary In a study of the neural processes that mediate visual attention in humans, 32-channel recordings of event-related potentials were obtained from 14 normal subjects while they performed a spatial attention task. The generator locations of the early C1, P1, and Nl components of the visual evoked response were estimated by means of topographic maps of voltage and current source density in conjunction with dipole modelling. The topography of the C1 component (ca. 85 ms post-stimulus) was consistent with a generator in striate cortex, and this component was unaffected by attention. In contrast, the P1 and Nl components (ca. 95 and 170ms) exhibited current density foci at scalp sites overlying lateral extrastriate cortex and were larger for attended stimuli than for unattended stimuli. The voltage topographies in the 75–175 ms latency range were modeled with a 5-dipole configuration consisting of a single striate dipole and left-right pairs of dipoles located in lateral extrastriate and inferior occipito-temporal areas. This model was found to account for the voltage topographies produced by both attended and unattended stimuli with low residual variance. These results support the proposal that visual-spatial attention modulates neural activity in extrastriate visual cortex but does not affect the initial evoked response in striate cortex.This study was supported by ONR Contract N00014-89-J-1806, by grants from NIMH (MH-25594), NINCDS (NS 17778), the Human Frontier Science Program, DGICYT (PM92-0128), and by a Fulbright scholarship to the first author.     

Spatially specific FMRI repetition effects in human visual cortex

The functional MRI (fMRI) response to a pair of identical, successively presented stimuli can result in a smaller signal than the presentation of two nonidentical stimuli. This "repetition effect" has become a frequently used tool to make inferences about neural selectivity in specific cortical areas. However, little is known about the mechanism(s) underlying the effect. In particular, despite many successful applications of the technique in higher visual areas, repetition effects in lower visual areas [e.g., primary visual cortex (V1)] have been more difficult to characterize. One property that is well understood in early visual areas is the mapping of visual field locations to specific areas of the cortex (i.e., retinotopy). We used the retinotopic organization of V1 to activate progressively different populations of neurons in a rapid fMRI experimental design. We observed a repetition effect (reduced signal) when localized stimulus elements were repeated in identical locations. We show that this effect is spatially tuned and largely independent of both interstimulus interval (100-800 ms) and the focus of attention. Using the same timing parameters for which we observed a large effect of spatial position, we also examined the response to orientation changes and observed no effect of an orientation change on the response to repeated stimuli in V1 but significant effects in other retinotopic areas. Given these results, we discuss the possible causes of these repetition effects as well as the implications for interpreting other experiments that use this potentially powerful imaging technique.     

Neuronal responses from beyond the classic receptive field in V1 of alert monkeys

Responses of primary visual cortex (V1) neurons to stimuli inside the classic receptive field (CRF) can be modulated by stimuli outside the CRF. We recently reported that responses of most V1 neurons to a line in the CRF center are inhibited by large surround-stimuli and that this modulation is stimulus selective. Here we report that a significant proportion of V1 neurons in alert monkeys respond directly to stimuli outside the CRF with very long latency and much reduced selectivity. When surround stimuli are presented alone, three response patterns can be distinguished in 153 single- or multiunits tested: (1) 31.4% have no significant response; (2) 50.3% show excitatory responses that are significantly higher than spontaneous activity. The average latency of these responses is about 145 ms, 2–3 times longer than center responses; (3) 18.3% show suppressed spontaneous activity after stimulus onset. The direct surround responses are found to be only weakly selective for the orientation of contextual lines, and not selective for other contextual patterns tested. While the outburst of responses to stimuli within the CRF is not affected by reducing stimulus duration from 500 ms to 50 ms, late excitatory surround responses are virtually eliminated. We propose that the late excitatory surround responses to extra-CRF stimulation alone are the reflection of feedback from higher cortical areas and may contribute to reduced contextual inhibition of cells in V1. This could play a role in figure-ground segregation. Electronic Publication     

Loss of attentional stimulus selection after extrastriate cortical lesions in macaques.

Many objects in natural visual scenes compete for attention. To identify the neural mechanisms necessary for visual attention, we made restricted lesions, affecting different quadrants of the visual field but leaving one quadrant intact, in extrastriate cortical areas V4 and TEO of two monkeys. Monkeys were trained to discriminate the orientation of a target grating surrounded by distracters. As distracter contrast increased, performance deteriorated in quadrants affected by V4 and TEO lesions, but not in the normal quadrant. Performance in affected quadrants was restored by increasing the contrast of the target relative to distracters. Thus, without V4 and TEO, visual attention is 'captured' by strong stimuli, regardless of their behavioral relevance.     

Stronger occipital cortical activation to lower than upper visual field stimuli Neuromagnetic recordings

 We recorded whole-scalp magnetoencephalographic (MEG) responses to black-and-white checkerboards to study whether the human cortical responses are quantitatively similar to stimulation of the lower and upper visual field at small, 0–6°, eccentricities. All stimuli evoked strongoccipital responses peaking at 50–100 ms (mean 75 ms). The activation was modeled with a single equivalent current dipole in the contralateral occipital cortex, close to the calcarine fissure, agreeing with an activation of the V1/V2 cortex. The dipole was, on average, twice as strong to lower than to upper field stimuli. Responses to hemifield stimuli that extended to both lower and upper fields resembled the responses to lower field stimuli in source current direction and strength. These results agree with psychophysical data, which indicate lower visual field advantage in complex visual processing. Parieto-occipital responses in the putative V6 complex were similar to lower and upper field stimuli. Received: 16 March 1998 / Accepted: 9 September 1998     

Combined activation and deactivation of visual cortex during tactile sensory processing

The involvement of occipital cortex in sensory processing is not restricted solely to the visual modality. Tactile processing has been shown to modulate higher-order visual and multisensory integration areas in sighted as well as visually deprived subjects; however, the extent of involvement of early visual cortical areas remains unclear. To investigate this issue, we employed functional magnetic resonance imaging in normally sighted, briefly blindfolded subjects with well-defined visuotopic borders as they tactually explored and rated raised-dot patterns. Tactile task performance resulted in significant activation in primary visual cortex (V1) and deactivation of extrastriate cortical regions V2, V3, V3A, and hV4 with greater deactivation in dorsal subregions and higher visual areas. These results suggest that tactile processing affects occipital cortex via two distinct pathways: a suppressive top-down pathway descending through the visual cortical hierarchy and an excitatory pathway arising from outside the visual cortical hierarchy that drives area V1 directly.     

Temporal analysis of the flow from V1 to the extrastriate cortex in humans

We previously examined the cortical processing in response to somatosensory, auditory and noxious stimuli, using magnetoencephalography in humans. Here, we performed a similar analysis of the processing in the human visual cortex for comparative purposes. After flash stimuli applied to the right eye, activations were found in eight cortical areas: the left medial occipital area around the calcarine fissure (primary visual cortex, V1), the left dorsomedial area around the parietooccipital sulcus (DM), the ventral (MOv) and dorsal (MOd) parts of the middle occipital area of bilateral hemispheres, the left temporo-occipito-parietal cortex corresponding to human MT/V5 (hMT), and the ventral surface of the medial occipital area (VO) of the bilateral hemispheres. The mean onset latencies of each cortical activity were (in ms): 27.5 (V1), 31.8 (DM), 32.8 (left MOv), 32.2 (right MOv), 33.4 (left MOd), 32.3 (right MOv), 37.8 (hMT), 46.9 (left VO), and 46.4 (right VO). Therefore the cortico-cortical connection time of visual processing at the early stage was 4-6 ms, which is very similar to the time delay between sequential activations in somatosensory and auditory processing. In addition, the activities in V1, MOd, DM, and hMT showed a similar biphasic waveform with a reversal of polarity after 10 ms, which is a common activation profile of the cortical activity for somatosensory, auditory, and pain-evoked responses. These results suggest similar mechanisms of the serial cortico-cortical processing of sensory information among all sensory areas of the cortex.     

Projections from the cytochrome oxidase modules of visual area V2 to the ventral posterior area in the macaque

The ventral part of the third visual cortical complex, the ventral posterior area (VP) or V3v, is located between the ventral half of visual areas V2 and V4. Because of its location and the physiological properties of its neurons, VP has been considered to be involved in the ventral stream visual areas. The ventral stream visual areas such as V4 and TEO receive projections from the cytochrome oxidase (CO)-rich thin stripes and CO-poor interstripe regions of V2; however, which CO-modules project to VP remains unclear. Moreover, it is not clear whether V1 projects to VP. We injected retrograde tracers into VP and found that VP receives projections from V2 neurons not only in the CO-rich thin stripes and CO-poor interstripe regions but also in the CO-rich thick stripes. We also confirmed the virtual absence of inputs from V1 to VP. These results support the hypothesis that VP constitutes a distinct extrastriate visual area and also suggest that, in addition to color and shape information, VP may also process visual information related to space and disparity.     

Modulation of cortical excitability can speed up blindsight but not improve it

Blindsight has been widely investigated and its properties documented. One property still debated and contested is the puzzling absence of phenomenal visual percepts of visual stimuli that can be detected with perfect accuracy. We investigated the possibility that phenomenal visual percepts of exogenous visual stimuli in patient GY might be induced by using transcranial direct current stimulation. High contrast and low contrast stimuli were presented as a moving grating in his blind hemifield. When left area MT/V5 was anodally stimulated during the presentation of high-contrast gratings, he never reported a phenomenal percept of a moving grating but showed perfect blindsight performance. When applied along with low contrast gratings, for which accuracy was titrated to 60–70 %, performance did not improve but responses were significantly faster. Cathodal stimulation had no effect. Results are explained in the framework of GY’s reorganized cortical connexions and oscillatory patterns known to be involved in awareness in GY. The apparent presence of phenomenal visual percepts in earlier studies is shown to be a semantic confusion about what he means when he says that he sees in his blind field.     

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.     

Orientation-selective adaptation to first- and second-order patterns in human visual cortex

Second-order textures-patterns that cannot be detected by mechanisms sensitive only to luminance changes-are ubiquitous in visual scenes, but the neuronal mechanisms mediating perception of such stimuli are not well understood. We used an adaptation protocol to measure neural activity in the human brain selective for the orientation of second-order textures. Functional MRI (fMRI) responses were measured in three subjects to presentations of first- and second-order probe gratings after adapting to a high-contrast first- or second-order grating that was either parallel or orthogonal to the probe gratings. First-order (LM) stimuli were generated by modulating the stimulus luminance. Second-order stimuli were generated by modulating the contrast (CM) or orientation (OM) of a first-order carrier. We used four combinations of adapter and probe stimuli: LM:LM, CM:CM, OM:OM, and LM:OM. The fourth condition tested for cross-modal adaptation with first-order adapter and second-order probe stimuli. Attention was diverted from the stimulus by a demanding task at fixation. Both first- and second-order stimuli elicited orientation-selective adaptation in multiple cortical visual areas, including V1, V2, V3, V3A/B, a newly identified visual area anterior to dorsal V3 that we have termed LO1, hV4, and VO1. For first-order stimuli (condition LM:LM), the adaptation was no larger in extrastriate areas than in V1, implying that the orientation-selective first-order (luminance) adaptation originated in V1. For second-order stimuli (conditions CM:CM and OM:OM), the magnitude of adaptation, relative to the absolute response magnitude, was significantly larger in VO1 (and for condition CM:CM, also in V3A/B and LO1) than in V1, suggesting that second-order stimulus orientation was extracted by additional processing after V1. There was little difference in the amplitude of adaptation between the second-order conditions. No consistent effect of adaptation was found in the cross-modal condition LM:OM, in agreement with psychophysical evidence for weak interactions between first- and second-order stimuli and computational models of separate mechanisms for first- and second-order visual processing.     

Functional degradation of extrastriate visual cortex in senescent rhesus monkeys

The receptive field properties of striate cortical (V1) cells degrade in senescent macaque monkeys. We have now carried out extracellular single unit studies of the receptive field properties of cells in extrastriate visual cortex (area V2) in very old rhesus (Macaca mulatta) monkeys. This study provides evidence that both the orientation and direction selectivities of V2 cells in old monkeys degrade significantly. Decreased selectivity is accompanied by increased visually driven and spontaneous responses. As a result, V2 cells in old animals exhibit markedly decreased signal-to-noise ratios. A significant degradation of neural function in extrastriate cortex may underlie the declines in higher order visual function that accompany normal aging.     

Neural responses in the primary visual cortex of the monkey during perceptual filling-in at the blind spot

The phenomenon of perceptual filling-in demonstrates that physical stimuli presented on the retina do not necessarily correspond to surface perception, and that our visual system has mechanisms with which to interpolate missing information in order to construct continuous surfaces. Among its various forms, filling-in at the blind spot is one of the most remarkable. To study the neural mechanisms involved in filling-in at the blind spot, we recently conducted a recording experiment aimed at determining whether the neurons in the primary visual cortex (V1) that represent the visual field corresponding to the blind spot are activated when filling-in occurs. We found that neurons located in deep layers of the V1, particularly layer 6, respond to large stimuli that cover the blind spot and induce perceptual filling-in. These neurons tended to have very large receptive fields, which extended out of the blind spot, and preferred relatively large stimuli. We believe that neurons in the V1 region representing the blind spot encode information essential for perceptual filling-in at the blind spot.     

Multisensory convergence in calcarine visual areas in macaque monkey.

The neural substrates of multisensory perception and integration are still obscure, especially at the cortical level. Alternative viewpoints emphasize (1) 'bottom-up' processes, where different modalities converge in higher order multisensory areas, or (2) 'top-down' projections from multimodal to unimodal areas. In this anatomic study, we use anterograde tracer injections in parietal (8 monkeys) and auditory (3 monkeys) association areas, and demonstrate direct projections to areas V1 and V2 in the calcarine fissure (i.e. the peripheral visual field representation). The laminar signature, with terminations in layers 1 and/or 6, could be consistent with feedback-type connections. A subset of connections from parietal areas, however, branch to both V1 and a ventral extrastriate area (TEO or TEp). Thus, the direct connections to early visual areas V1 and V2 may well operate in conjunction with polysynaptic pathways in a densely parallel network.     

Anticipatory attention to verbal and non-verbal stimuli is reflected in a modality-specific SPN

The time estimation paradigm allows the recording of anticipatory attention for an upcoming stimulus unconfounded by any anticipatory motor activity. Three seconds after a warning signal (WS) subjects have to press a button. A button press within a time window from 2,850 ms to 3,150 ms after the WS is considered ‘correct’, a movement prior to 2,850 ms after the WS is labelled ‘too early’ and a movement after 3,150 ms is labelled ‘too late’. Two seconds after the button press a Knowledge of Results (KR) stimulus is presented, informing the subject about the correctness of the response. Stimulus Preceding Negativity (SPN) is a slow wave which is recorded prior to the presentation of the KR stimulus. The SPN has a right hemisphere preponderance and is based upon activity in a network in which prefrontal cortex, the insula Reili and the parietal cortex are crucial. In the present study we asked two questions: (1) does the SPN show modality specificity and (2) does the use of verbal KR stimuli influence the right hemisphere preponderance? Auditory and visual stimuli were presented, in a verbal mode and in a non-verbal mode. SPN amplitudes prior to visual stimuli were larger over the visual cortex than prior to auditory stimuli. SPN amplitudes prior to auditory stimuli were larger over the frontal areas than prior to visual stimuli. The use of verbal stimuli did not influence the right hemisphere preponderance. We concluded that apart from the supramodal effect of KR stimuli in general, there is (first) a modality-specific activation of the relevant sensory cortical areas. The supramodal network underlying the attention for and the use of KR information is activated either from different sensory areas or from language processing cortical areas.     

Simultaneous recordings of visual evoked potentials and BOLD MRI activations in response to visual motion processing

Visual motion processing in humans was studied by simultaneous 32-channel electroencephalography (EEG) recordings of visual evoked potentials and BOLD MRI activations at 2.9 T. The paradigms compared three different random dot patterns (12 s duration) with stationary random dots (18 s) or with each other. The stimuli represented pattern reversal (500 ms switches between two stationary patterns), motion onset (200 ms of starfield motion followed by 1000 ms of stationary dots) and motion reversal (reversal of moving starfield directions every 1000 ms). Whereas motion-evoked visual potentials, and in particular the N2 component in occipito-temporal channels, were most prominent for motion onset, the most extended BOLD MRI activations and strongest signal changes in V5/MT+ were obtained in response to motion reversal. These apparently contradictory findings most likely reflect different physiological aspects of the neural activity associated with visual motion processing. For example, desynchronized activity of subpopulations of cortical neurons inside V5/MT+ is expected to attenuate visual evoked potentials in scalp recordings while continuously driving metabolic demands that lead to sustained BOLD MRI responses. The understanding of the physiological correlates and neural processes underlying either technique is fundamental to exploring fully the potential of combined EEG-MRI for studying human brain function at both high temporal and spatial resolution.