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Processing of second-order stimuli in the visual cortex.

Naturally occurring visual stimuli are rich in examples of objects delineated from their backgrounds simply by differences in luminance, so-called first-order stimuli, as well as those defined by differences of contrast or texture, referred to as second-order stimuli. Here we provide a brief overview of visual cortical processing of second-order stimuli, as well as some comparative background on first-order processing, concentrating on single-unit neurophysiology, but also discussing relationships to human psychophysics and to neuroimaging. The selectivity of visual cortical neurons to orientation, spatial frequency, and direction of movement of first-order, luminance-defined stimuli is conventionally understood in terms of simple linear filter models, albeit with some minor nonlinearities such as thresholding and gain control. However, these kinds of models fail entirely to account for responses of neurons to second-order stimuli such as contrast envelopes, illusory contours, or texture borders. Second-order stimuli constructed from sinusoidal components have been used to analyze the neurophysiological mechanisms of such responses; these experiments demonstrate that the same neuron can exhibit three distinct kinds of tuning to spatial frequency, and also to orientation. These results can be understood in terms of a type of nonlinear 'filter-->rectify-->filter' model, which has been widely used in human psychophysics. Finally, several general issues will be discussed, including potential artifacts in experiments with second-order stimuli, and strategies for avoiding or controlling for them; caveats about definitions of first- vs. second-order mechanisms and stimuli; the concept of form-cue invariance; and the functional significance of second-order processing.

Animals↗

Feedforward, horizontal, and feedback processing in the visual cortex.

The cortical visual system consists of many richly interconnected areas. Each area is characterized by more or less specific receptive field tuning properties. However, these tuning properties reflect only a subset of the interactions that occur within and between areas. Neuronal responses may be modulated by perceptual context or attention. These modulations reflect lateral interactions within areas and feedback from higher to lower areas. Recent work is beginning to unravel how horizontal and feedback connections each contribute to modulatory effects and what the role of these modulations is in vision. Whereas receptive field tuning properties reflect feedforward processing, modulations evoked by horizontal and feedback connections may reflect the integration of information that underlies perception.

Animals↗

Retinotopic organization of the guinea pig's visual cortex.

Under anaesthesia the right visual cortex of the guinea pig was investigated with 1.5 M potassium citrate-filled glass microelectrodes. Single unit and small unit cluster response showed an organized three-part representation of the contralateral visual field on the animal's visual cortex. The major central division (V1) had the representation of a nasotemporally elongated visual field. This visual field extended for about 110 degrees horizontally and for about 70 degrees vertically. The nasal visual field was represented laterally on the cortex and the lower visual field anteriorly. The visual field representation was not uniformly magnified in V1; the magnification of the nasal field was higher than the rest of the visual field. On either side of V1, the guinea pig's cortex had two additional visually responsive strips. The strip V2L, situated lateral to V1, had a condensed representation of about 40 degrees of the animal's nasal visual field and mirror-imaged the visual field representation of the adjacent V1. The strip V2M, situated medial to V1, had a similar representation of about 40 degrees of the animal's temporal visual field and mirror-imaged the visual field representation of the area V1 adjacent to it. A binocularly responsive zone of cortex was observed on either side of the boundary between the areas V1 and V2L, representing between 10 degrees and 15 degrees of the nasal visual field on each side of the boundary line. Investigation of the retinal ganglion cell distribution of the animal showed a nasotemporally oriented 'visual streak' with a high ganglion cell density per unit area of the retina, near the optic disc. Away from the 'visual streak' the density of the ganglion cells of the retina diminished progressively. The configuration of the 'visual streak' and the general pattern of the ganglion cell distribution in the rest of the retina coincided with the asymmetry in the magnification of representation of the animal's visual field on the cortex.

Animals↗

Comparison of serotonin 5-HT1 receptors and innervation in the visual cortex of normal and dark-reared cats.

The visual cortical serotoninergic system was compared in normal and dark-reared cats to determine whether visual experience is necessary for its normal development. In vitro receptor binding of [3H]5-HT indicated an increase in 5-HT1 receptor number in dark-reared cats with no change in affinity. This elevation was specific to the visual cortex and no changes were found in the frontal cortex as a result of dark rearing. Autoradiographic histology revealed that in the normal cat visual cortex, 5-HT1 receptors were present in all cortical layers and were slightly more dense in supragranular and infragranular layers. In dark-reared cats, there was a marked elevation in receptor density in supragranular and infragranular layers and little change within layer IV. Immunohistochemical techniques (anti-5-HT) were used to compare serotoninergic innervation in the visual cortex of normal and dark-reared cats. In normal cat visual cortex, serotonin fibers were most dense in the superficial layers (I-III), least dense in layers IV and VI, and intermediate in layer V. No differences were found between normal and dark-reared cats in the laminar distribution or density of serotoninergic innervation. These results indicate that visual experience is necessary for the normal development of the visual cortical serotonin system. The findings that the effects of dark rearing were specific to the visual cortex and that within the visual cortex these effects were specific to supra- and infragranular layers are consistent with a possible role for serotonin in the prolonged physiological plasticity that occurs in the visual cortex of dark-reared cats.

Animals↗

Distribution of somatostatin receptors in the cat and monkey visual cortex demonstrated by in vitro receptor autoradiography.

Somatostatin (SRIF, S14) receptors in the cat and monkey visual cortex were visualized by means of in vitro autoradiography with an iodinated agonist of SRIF, [125I-Tyr0,DTrp8]S14. The kinetics, performed on tissue sections, revealed an apparently single, saturable site (KD = 3.92 +/- 0.31 10(-10) M for the cat, and 3.82 +/- 0.28 10(-10) M for the monkey visual cortex) with pharmacological specificity for S14 and [DTrp]-substituted S14. Autoradiography, performed on frontal sections of the cat and monkey visual cortex, revealed a heterogeneous regional and laminar distribution of SRIF receptors. In cat areas 17, 18, and 19, SRIF receptors occur mainly in the supragranular layers, although small interareal and intra-areal differences are observed. The infragranular layers (V-VI) in area 19 contain a significantly higher proportion of SRIF receptors compared to both areas 17 and 18. In the antero- (AMLS) and posteromedial lateral suprasylvian area (PMLS), layers V and VI contain the highest proportion of SRIF receptors. This latter pattern is also observed in the area prostriata medially adjoining area 17 in the splenial sulcus. In the monkey visual cortex, areas 17 and 18 exhibit similar distribution patterns, SRIF receptors being primarily concentrated in layers V and VI. Neither in the cat nor the monkey visual cortex could we observe significant differences in SRIF receptor distribution between different retinotopic subdivisions within one area.

Animals↗

Affective picture perception: gender differences in visual cortex?

Activity in extrastriate visual cortex is greater when people view emotional relative to neutral pictures. Prior brain imaging and psychophysiological work has further suggested a bias for men to react more strongly to pleasant pictures, and for women to react more strongly to unpleasant pictures. Here we investigated visual cortical activity using fMRI in 28 men and women during picture viewing. Men and women showed reliably greater visual cortical reactivity during both pleasant and unpleasant pictures, relative to neutral, consistent with the view that the motivational relevance of visual stimuli directs attention and enhances elaborative perceptual processing. However, men did show greater extrastriate activity than women specifically during erotic picture perception, possibly reflecting a gender-specific visual mechanism for sexual selection.

Adolescent↗

Enduring critical period plasticity visualized by transcranial flavoprotein imaging in mouse primary visual cortex.

Experience-dependent plasticity in the visual cortex was investigated using transcranial flavoprotein fluorescence imaging in mice anesthetized with urethane. On- and off-responses in the primary visual cortex were elicited by visual stimuli. Fluorescence responses and field potentials elicited by grating patterns decreased similarly as contrasts of visual stimuli were reduced. Fluorescence responses also decreased as spatial frequency of grating stimuli increased. Compared with intrinsic signal imaging in the same mice, fluorescence imaging showed faster responses with approximately 10 times larger signal changes. Retinotopic maps in the primary visual cortex and area LM were constructed using fluorescence imaging. After monocular deprivation (MD) of 4 d starting from postnatal day 28 (P28), deprived eye responses were suppressed compared with nondeprived eye responses in the binocular zone but not in the monocular zone. Imaging faithfully recapitulated a critical period for plasticity with maximal effects of MD observed around P28 and not in adulthood even under urethane anesthesia. Visual responses were compared before and after MD in the same mice, in which the skull was covered with clear acrylic dental resin. Deprived eye responses decreased after MD, whereas nondeprived eye responses increased. Effects of MD during a critical period were tested 2 weeks after reopening of the deprived eye. Significant ocular dominance plasticity was observed in responses elicited by moving grating patterns, but no long-lasting effect was found in visual responses elicited by light-emitting diode light stimuli. The present results indicate that transcranial flavoprotein fluorescence imaging is a powerful tool for investigating experience-dependent plasticity in the mouse visual cortex.

Animals↗

Rabbit cingulate cortex: cytoarchitecture, physiological border with visual cortex, and afferent cortical connections of visual, motor, postsubicular, and intracingulate origin.

The connections of cingulate cortex with visual, motor, and parahippocampal cortices in the rabbit brain are evaluated by using a modified Brodmann cytoarchitectural scheme, electrophysiological mapping techniques, and the pathway tracers horseradish peroxidase (HRP) and tritiated amino acids. Rabbit cingulate cortex can be divided into areas 25, 24, and 29. Area 29 is of particular interest because area 29d has a lateral extension with a granular layer IV, area 29b has a caudal extension in which the connections differ from anterior area 29b, and there is a prominent area 29e. Cytoarchitectural delineation of the lateral border of area 29d with area 17 closely approximates the medial edge of the visual field representation in area 17 as determined electrophysiologically. The main interconnections between visual and cingulate cortices occur between cingulate areas 24b and 29d and visual areas 18 and medial parts of area 17. Projections between areas 29d and 18 are organized in a loose topographic fashion with rostral parts of each and caudal parts of each being reciprocally connected. Neurons mainly in superficial layer II-III of areas 17 and 18 project to layer I of area 29d, while the reciprocal projection originates from neurons in layer V of area 29d and project mainly to layer I of areas 17 and 18. The medial portion of motor area 8 projects to areas 18 and 29d and has a smaller projection to area 17. Postsubicular area 48 is reciprocally connected with area 29d, and it also projects to areas 29b and c. The subiculum projects to areas 29a and 29c but only to the anterior two-thirds of area 29b not the posterior one-third. Rostral area 29d receives the most extensive intrinsic cingulate projections including those from all major cytoarchitectural divisions. Interconnections between areas 29d and 29b appear to be topographically organized in the rostrocaudal plane. Area 29c projects more heavily to area 29b than vice versa. Finally area 29d projects mainly to area 24b in anterior cingulate cortex. In conclusion, rostral area 29d has extensive connections with visual areas 17 and 18, motor area 8, and all subdivisions of cingulate cortex. In light of these connections, it may play a pivotal role in associative functions of the rabbit cerebral cortex including visuomotor integration.

Animals↗

Callosal projections in the visual cortex and the vertical meridian of the visual field in the albino rat.

Studies using electrophysiological and HRP-labeling techniques showed that the lateral border of physiologically determined primary visual cortex coincides with the cytoarchiectonically defined area 17/18a border. The dense callosal projections are distributed in a zone, about 1.5 mm wide, along this border, which lies in the callosal zone, about 1/4-1/3 of the zone width from its lateral limit. There are two representations of the vertical meridian of the visual field, one in the proper of area 17, about 1/3 of the zone width from its medial limit, the other in area 18a, at about the lateral zone limit.

Animals↗

Interactions between attention, context and learning in primary visual cortex.

Attention in early visual processing engages the higher order, context dependent properties of neurons. Even at the earliest stages of visual cortical processing neurons play a role in intermediate level vision - contour integration and surface segmentation. The contextual influences mediating this process may be derived from long range connections within primary visual cortex (V1). These influences are subject to perceptual learning, and are strongly modulated by visuospatial attention, which is itself a learning dependent process. The attentional influences may involve interactions between feedback and horizontal connections in V1. V1 is therefore a dynamic and active processor, subject to top-down influences.

Animals↗

Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex.

In the primary visual cortex of macaque monkeys, laminar and columnar axonal specificity are correlated with functional differences between locations. We describe evidence that embedded within this anatomical framework is finer specificity of functional connections. Photostimulation-based mapping of functional input to 31 layer 3B neurons revealed that input sources to individual cells were highly diverse. Although some input differences were correlated with neuronal anatomy, no 2 neurons received excitatory input from the same cortical layers. Thus, input diversity reveals far more cell types than does anatomical diversity. This implies relatively little functional redundancy; despite trends related to laminar or columnar position, pools of neurons contributing uniquely to visual processing are likely relatively small. These results also imply that similarities in the anatomy of circuits in different cortical areas or species may not indicate similar functional connectivity.

Animals↗

In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex.

Cortical representations of visual information are modified by an animal's visual experience. To investigate the mechanisms in mice, we replaced the coding part of the neural activity-regulated immediate early gene Arc with a GFP gene and repeatedly monitored visual experience-induced GFP expression in adult primary visual cortex by in vivo two-photon microscopy. In Arc-positive GFP heterozygous mice, the pattern of GFP-positive cells exhibited orientation specificity. Daily presentations of the same stimulus led to the reactivation of a progressively smaller population with greater reactivation reliability. This adaptation process was not affected by the lack of Arc in GFP homozygous mice. However, the number of GFP-positive cells with low orientation specificity was greater, and the average spike tuning curve was broader in the adult homozygous compared to heterozygous or wild-type mice. These results suggest a physiological function of Arc in enhancing the overall orientation specificity of visual cortical neurons during the post-eye-opening life of an animal.

Animals↗

The contribution of noise to contrast invariance of orientation tuning in cat visual cortex.

Feedforward models of visual cortex appear to be inconsistent with a well-known property of cortical cells: contrast invariance of orientation tuning. The models' fixed threshold broadens orientation tuning as contrast increases, whereas in real cells tuning width is invariant with contrast. We have compared the orientation tuning of spike and membrane potential responses in single cells. Both are contrast invariant, yet a threshold-linear relation applied to the membrane potential accurately predicts the orientation tuning of spike responses. The key to this apparent paradox lies in the noisiness of the membrane potential. Responses that are subthreshold on average are still capable of generating spikes on individual trials. Unlike the iceberg effect, contrast invariance remains intact even as threshold narrows orientation selectivity. Noise may, by extension, smooth the average relation between membrane potential and spike rate throughout the brain.

Action Potentials↗

Geometrical computations explain projection patterns of long-range horizontal connections in visual cortex.

Neurons in primary visual cortex respond selectively to oriented stimuli such as edges and lines. The long-range horizontal connections between them are thought to facilitate contour integration. While many physiological and psychophysical findings suggest that collinear or association field models of good continuation dictate particular projection patterns of horizontal connections to guide this integration process, significant evidence of interactions inconsistent with these hypotheses is accumulating. We first show that natural random variations around the collinear and association field models cannot account for these inconsistencies, a fact that motivates the search for more principled explanations. We then develop a model of long-range projection fields that formalizes good continuation based on differential geometry. The analysis implicates curvature(s) in a fundamental way, and the resulting model explains both consistent data and apparent outliers. It quantitatively predicts the (typically ignored) spread in projection distribution, its nonmonotonic variance, and the differences found among individual neurons. Surprisingly, and for the first time, this model also indicates that texture (and shading) continuation can serve as alternative and complementary functional explanations to contour integration. Because current anatomical data support both (curve and texture) integration models equally and because both are important computationally, new testable predictions are derived to allow their differentiation and identification.

Animals↗

Computational modeling of orientation tuning dynamics in monkey primary visual cortex.

In the primate visual pathway, orientation tuning of neurons is first observed in the primary visual cortex. The LGN cells that comprise the thalamic input to V1 are not orientation tuned, but some V1 neurons are quite selective. Two main classes of theoretical models have been offered to explain orientation selectivity: feedforward models, in which inputs from spatially aligned LGN cells are summed together by one cortical neuron; and feedback models, in which an initial weak orientation bias due to convergent LGN input is sharpened and amplified by intracortical feedback. Recent data on the dynamics of orientation tuning, obtained by a cross-correlation technique, may help to distinguish between these classes of models. To test this possibility, we simulated the measurement of orientation tuning dynamics on various receptive field models, including a simple Hubel-Wiesel type feedforward model: a linear spatiotemporal filter followed by an integrate-and-fire spike generator. The computational study reveals that simple feedforward models may account for some aspects of the experimental data but fail to explain many salient features of orientation tuning dynamics in V1 cells. A simple feedback model of interacting cells is also considered. This model is successful in explaining the appearance of Mexican-hat orientation profiles, but other features of the data continue to be unexplained.

Action Potentials↗

Relationship between excitation and inhibition underlying size tuning and contextual response modulation in the cat primary visual cortex.

In the primary visual cortex (V1), the single-neuron response to a grating stimulus placed in the classical receptive field (CRF) is suppressed by a similar stimulus presented in the CRF surround. To assess the input mechanism underlying the surround suppression, we tested the effects of iontophoretically administered GABA(A)-receptor antagonist, bicuculline methiodide (BMI), for the 46 V1 neurons in anesthetized cats. First, the stimulus-size tuning curves were studied, with or without BMI administration, for each neuron by changing the size of the grating patch. During the BMI administration, the shape of the normalized size tuning curve did not change considerably. Second, the dependency of surround suppression on the orientation of the surround grating was examined. In the control, the surround suppression showed the clear orientation tuning that peaked at an orientation the same as the optimal orientation of the CRF response. The BMI administration did not change the orientation dependency of surround suppression. We also estimated the relative contribution of excitation and inhibition to the size and orientation tuning of surround suppression. It was concluded that cortical excitation and inhibition were well balanced, having similar tuning profiles for both stimulus size and orientation of the surround grating. Furthermore, surround stimuli used for V1 neurons suppressed the CRF response of neurons in the lateral geniculate nucleus. These results suggest that surround suppression is not primarily attributable to the intracortical inhibition, but because of a reduction of thalamocortical inputs, which drive the cortical excitation and inhibition, and a subsequent decrease in the cortical excitatory interactions.

Animals↗

Ocular dominance in anterior visual cortex in a child demonstrated by the use of fMRI.

Negative signal changes in the visual cortex have been observed during visual stimulation when performing functional magnetic resonance imaging (fMRI) in children. This report investigated whether the ocular dominance, which has been demonstrated in the contralateral anterior visual cortex in adults, could be observed in a child by the use of fMRI. A 5-year-old child was studied using fMRI at 1.5 T during alternating monocular visual stimulation under sedation with morphine and pentobarbital. The functional images were motion corrected, and statistical parametric maps were made by contrasting the left or right eye stimulation conditions vs the right or left eye stimulation conditions, respectively, at each voxel. Areas with negative signal changes were found on the left anterior visual cortex during monocular visual stimulation of the right eye and vice versa. There was no area with negative or positive signal change on the ipsilateral visual cortex to the stimulated eye and no area with positive signal change on the contralateral visual cortex. Contralateral ocular dominance of anterior visual cortex similar to that of adults was demonstrated in this child with a negative correlation with the visual stimulus. This finding suggests that peripheral visual fields are represented in the anterior visual cortex of 5-year-old children.

Child, Preschool↗

Spatiotemporal patterns of excitation and inhibition evoked by the horizontal network in layer 2/3 of ferret visual cortex.

The horizontal network in visual cortex layer 2/3 is implicated in numerous psychophysical and physiological properties. To investigate the spatial and temporal distribution of excitation and inhibition evoked by this network, we used voltage-sensitive dyes to image the responses to focal electrical stimulation in tangential slices of ferret visual cortex layer 2/3. The resulting optical patterns included a diffuse zone of activation near the stimulation site and numerous ovoid domains throughout the slice. In contrast to the fixed anatomy of the horizontal connections, substantial shifts in both space and time were evident in the distribution of population-based neuronal activity during stimulus trains. Both of these shifts relied on inhibitory synaptic potentials, suggesting that inhibition driven by horizontal connections sculpts the distribution of activity in this cortical network.

Animals↗