Image processing in the primary visual cortex

INTRODUCTION: Area 17 or the primary visual area forms the first link in the chain of cerebral analysis of a visual image. The neurones forming the primary visual cortex are characterized by the extreme precision of their connections, functional specialization and hierarchic organization. The spatial precision of the connections within the system for vision permit retinotopic representation in the visual cortex, so that each point of the retina is projected into a specific area of the cortex. The cortical neurones which analyze the characteristics of the image situated in a precise zone of the visual field are themselves organized into a basic functional unit known as a hypercolumn. Within each hypercolumn there are various columnar cell systems with receptive fields having similar characteristics. Thus, each hypercolumn is made up of multiple orientation columns, two ocular dominance columns and 'blob' regions. All these systems permit the analysis of different aspects of the image. The neurones belonging to the orientation columns are sensitive to the orientation, spatial frequency and movement of a visual stimulus; those of the 'blob' regions to colour, and the binocular neurones of the ocular dominance columns to depth. Within each column, the hierarchical pattern of neurone interconnections determines the successive appearance of cells with receptive fields having new properties.     

Immunohistochemical localiztion of homocysteate in human primary visual cortex

Polyclonal and monoclonal anti-homocysteate antibodies were used with a postembedding immunohistochemical method for light microscopy to localize homocysteate-like immunoreactivity in human primary visual cortex. Densely accumulated dots of diverse size resembling astrocytic processes were labelled in supragranular layers, mainly in layers I and II. Some glial elements intermingled with fibre bundles in the white matter, and astrocytic endfeet in the vicinity of capillaries were also stained. In addition, very few round or elongated neuronal cell bodies in layer IVc were intensely homocysteate immunoreactive. These observations extend to human primary visual cortex previous studies on the preferential localization of L-homocysteate in glia.     

Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity

The origin of orientation selectivity in visual cortical responses is a central problem for understanding cerebral cortical circuitry. In cats, many experiments suggest that orientation selectivity arises from the arrangement of lateral geniculate nucleus (LGN) afferents to layer 4 simple cells. However, this explanation is not sufficient to account for the contrast invariance of orientation tuning. To understand contrast invariance, we first characterize the input to cat simple cells generated by the oriented arrangement of LGN afferents. We demonstrate that it has two components: a spatial-phase-specific component (i.e., one that depends on receptive field spatial phase), which is tuned for orientation, and a phase-nonspecific component, which is untuned. Both components grow with contrast. Second, we show that a correlation-based intracortical circuit, in which connectivity between cell pairs is determined by the correlation of their LGN inputs, is sufficient to achieve well tuned, contrast-invariant orientation tuning. This circuit generates both spatially opponent, "antiphase" inhibition ("push-pull"), and spatially matched, "same-phase" excitation. The inhibition, if sufficiently strong, suppresses the untuned input component and sharpens responses to the tuned component at all contrasts. The excitation amplifies tuned responses. This circuit agrees with experimental evidence showing spatial opponency between, and similar orientation tuning of, the excitatory and inhibitory inputs received by a simple cell. Orientation tuning is primarily input driven, accounting for the observed invariance of tuning width after removal of intracortical synaptic input, as well as for the dependence of orientation tuning on stimulus spatial frequency. The model differs from previous push-pull models in requiring dominant rather than balanced inhibition and in predicting that a population of layer 4 inhibitory neurons should respond in a contrast-dependent manner to stimuli of all orientations, although their tuning width may be similar to that of excitatory neurons. The model demonstrates that fundamental response properties of cortical layer 4 can be explained by circuitry expected to develop under correlation-based rules of synaptic plasticity, and shows how such circuitry allows the cortex to distinguish stimulus intensity from stimulus form.     

Independent component analysis of natural image sequences yields spatio-temporal filters similar to simple cells in primary visual cortex

Simple cells in the primary visual cortex process incoming visual information with receptive fields localized in space and time, bandpass in spatial and temporal frequency, tuned in orientation, and commonly selective for the direction of movement. It is shown that performing independent component analysis (ICA) on video sequences of natural scenes produces results with qualitatively similar spatio-temporal properties. Whereas the independent components of video resemble moving edges or bars, the independent component filters, i.e. the analogues of receptive fields, resemble moving sinusoids windowed by steady Gaussian envelopes. Contrary to earlier ICA results on static images, which gave only filters at the finest possible spatial scale, the spatio-temporal analysis yields filters at a range of spatial and temporal scales. Filters centred at low spatial frequencies are generally tuned to faster movement than those at high spatial frequencies.     

Simultaneous oxygenation and perfusion imaging study of functional activity in primary visual cortex at different visual stimulation frequency: quantitative correlation between BOLD and CBF changes

A relationship between regional cerebral blood flow (CBF) and blood oxygenation level dependent (BOLD) changes in the primary visual cortex (V1) at varied visual stimulation frequency has been examined quantitatively using the multislice FAIR technique. A linear correlation in the common activation areas between functional BOLD and CBF maps was observed. This supports the hypothesis that the task-stimulated BOLD changes in microvasculature are correlated with the CBF changes that presumably reflect the degree of neuronal activity. The linear correlation coefficients for intrasubject comparisons are more significant than those for intersubject comparisons. This suggests that using intrasubject comparisons for quantitative studies of neuronal activity related to different task stimuli and task performances should be more reliable than using intersubject comparisons.     

A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex

Cortical synapses exhibit several forms of short-term plasticity, but the contribution of this plasticity to visual response dynamics is unknown. In part, this is because the simple patterns of stimulation used to probe plasticity in vitro do not correspond to patterns of activity that occur in vivo. We have developed a method of quantitatively characterizing short-term plasticity at cortical synapses that permits prediction of responses to arbitrary patterns of stimulation. Synaptic responses were recorded intracellularly as EPSCs and extracellularly as local field potentials in layer 2/3 of rat primary visual cortical slices during stimulation of layer 4 with trains of electrical stimuli containing random mixtures of frequencies. Responses exhibited complex dynamics that were well described by a simple three-component model consisting of facilitation and two forms of depression, a stronger form that decayed exponentially with a time constant of several hundred milliseconds and a weaker, but more persistent, form that decayed with a time constant of several seconds. Parameters obtained from fits to one train were used to predict accurately responses to other random and constant frequency trains. Control experiments revealed that depression was not caused by a decrease in the effectiveness of extracellular stimulation or by a buildup of inhibition. Pharmacological manipulations of transmitter release and postsynaptic sensitivity suggested that both forms of depression are mediated presynaptically. These results indicate that firing evoked by visual stimuli is likely to cause significant depression at cortical synapses. Hence synaptic depression may be an important determinant of the temporal features of visual cortical responses.     

Temporal dynamics of chromatic tuning in macaque primary visual cortex

The ability to distinguish colour from intensity variations is a difficult computational problem for the visual system because each of the three cone photoreceptor types absorb all wavelengths of light, although their peak sensitivities are at relatively short (S cones), medium (M cones), or long (L cones) wavelengths. The first stage in colour processing is the comparison of the outputs of different cone types by spectrally opponent neurons in the retina and upstream in the lateral geniculate nucleus. Some neurons receive opponent inputs from L and M cones, whereas others receive input from S cones opposed by combined signals from L and M cones. Here we report how the outputs of the L/M- and S-opponent geniculate cell types are combined in time at the next stage of colour processing, in the macaque primary visual cortex (V1). Some V1 neurons respond to a single chromatic region, with either a short (68-95 ms) or a longer (96-135 ms) latency, whereas others respond to two chromatic regions with a difference in latency of 20-30 ms. Across all types, short latency responses are mostly evoked by L/M-opponent inputs whereas longer latency responses are evoked mostly by S-opponent inputs. Furthermore, neurons with late S-cone inputs exhibit dynamic changes in the sharpness of their chromatic tuning over time. We propose that the sparse, S-opponent signal in the lateral geniculate nucleus is amplified in area V1, possibly through recurrent excitatory networks. This results in a delayed, sluggish cortical S-cone signal which is then integrated with L/M-opponent signals to rotate the lateral geniculate nucleus chromatic axes.     

A local circuit approach to understanding integration of long-range inputs in primary visual cortex

Integration of inputs by cortical neurons provides the basis for the complex information processing performed in the cerebral cortex. Here, we have examined how primary visual cortical neurons integrate classical and nonclassical receptive field inputs. The effect of nonclassical receptive field stimuli and, correspondingly, of long-range intracortical inputs is known to be context-dependent: the same long-range stimulus can either facilitate or suppress responses, depending on the level of local activation. By constructing a large-scale model of primary visual cortex, we demonstrate that this effect can be understood in terms of the local cortical circuitry. Each receptive field position contributes both excitatory and inhibitory inputs; however, the inhibitory inputs have greater influence when overall receptive field drive is greater. This mechanism also explains contrast-dependent modulations within the classical receptive field, which similarly switch between excitatory and inhibitory. In order to simplify analysis and to explain the fundamental mechanisms of the model, self-contained modules that capture nonlinear local circuit interactions are constructed. This work supports the notion that receptive field integration is the result of local processing within small groups of neurons rather than in single neurons.     

Figure-ground activity in primary visual cortex is suppressed by anesthesia

By means of their small receptive fields (RFs), neurons in primary visual cortex perform highly localized analyses of the visual scene, far removed from our normal unified experience of vision. Local image elements coded by the RF are put into more global context, however, by means of modulation of the responses of the V1 neurons. Contextual modulation has been shown to follow closely the perceptual interpretation of the scene as a whole. This would suggest that some aspects of contextual modulation can be recorded only in awake and perceiving animals. In this study, multi-unit activity was recorded with implanted electrodes from primary visual cortex of awake, fixating monkeys viewing textured displays in which figure and ground regions were segregated by differences in either orientation or motion. Contextual modulation was isolated from local RF processing, by keeping RF stimulation identical across trials while sampling responses for various positions of the RF relative to figure and ground. Contextual modulation was observed to unfold spatially and temporally in a way that closely resembles the figure-ground percept. When recording was repeated, but with the animals anesthetized, the figure-ground related modulatory activity was selectively suppressed. RF tuning properties, however, remained unaffected. The results show that the modulatory activity is functionally distinct from the RF properties. V1 thus hosts distinct regimes of activity that are mediated by separate mechanisms and that depend differentially on the animal being awake or anesthetized.     

Age-dependent sparing of visual function after bilateral lesions of primary visual cortex.

Bilateral lesions of primary visual cortex (PVC) sustained early in life induce the visual system to undergo structural and functional reorganization and produce modified neuronal networks capable of mediating visual abilities that would be impaired if the lesions occurred in adulthood. Reorganization after early lesion is also accompanied by degeneration of the lateral geniculate nucleus of the thalamus, and 90% of beta retinal ganglion cells die via retrograde degeneration. It is unclear whether the high potential of the system to reorganize after early lesion could overcome the effects of beta retinal ganglion cell death. Visual acuity, which depends on an intact beta-cell array, was impaired in cats that underwent PVC lesions on postnatal day 1 and indicated that neuroplastic potential was insufficient to overcome early lesion-induced maladaptive plasticity. Animals with lesions made at 1 month of age, a stage accompanied by high levels of neuroplastic potential but no death of beta cells, achieved acuity measures equivalent to intact animals. The authors conclude that visual signals are rerouted to subserve functionality when the lesion is made at 1 month of age, but not at 1 day of age. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A neural model of contour integration in the primary visual cortex

Experimental observations suggest that contour integration may take place in V1. However, there has yet to be a model of contour integration that uses only known V1 elements, operations, and connection patterns. This article introduces such a model, using orientation selective cells, local cortical circuits, and horizontal intracortical connections. The model is composed of recurrently connected excitatory neurons and inhibitory interneurons, receiving visual input via oriented receptive fields resembling those found in primary visual cortex. Intracortical interactions modify initial activity patterns from input, selectively amplifying the activities of edges that form smooth contours in the image. The neural activities produced by such interactions are oscillatory and edge segments within a contour oscillate in synchrony. It is shown analytically and empirically that the extent of contour enhancement and neural synchrony increases with the smoothness, length, and closure of contours, as observed in experiments on some of these phenomena. In addition, the model incorporates a feedback mechanism that allows higher visual centers selectively to enhance or suppress sensitivities to given contours, effectively segmenting one from another. The model makes the testable prediction that the horizontal cortical connections are more likely to target excitatory (or inhibitory) cells when the two linked cells have their preferred orientation aligned with (or orthogonal to) their relative receptive field center displacements.     

Object-based attention in the primary visual cortex of the macaque monkey

Typical natural visual scenes contain many objects, which need to be segregated from each other and from the background. Present theories subdivide the processes responsible for this segregation into a pre-attentive and attentive system. The pre-attentive system segregates image regions that 'pop out' rapidly and in parallel across the visual field. In the primary visual cortex, responses to pre-attentively selected image regions are enhanced. When objects do not segregate automatically from the rest of the image, the time-consuming attentive system is recruited. Here we investigate whether attentive selection is also associated with a modulation of firing rates in area V1 of the brain in monkeys trained to perform a curve-tracing task. Neuronal responses to the various segments of a target curve were simultaneously enhanced relative to responses evoked by a distractor curve, even if the two curves crossed each other. This indicates that object-based attention is associated with a response enhancement at the earliest level of the visual cortical processing hierarchy.     

Serotonin inhibits the induction of long-term potentiation in rat primary visual cortex

1. The effect of serotonin (5-hydroxytryptamine; 5-HT) on the induction of long-term potentiation (LTP) in rat visual cortex was investigated by using slice preparations in vitro. 2. Bath application of 5-HT (0.1-10 microM) did not affect the baseline synaptic potentials evoked by single-pulse test stimulation, but inhibited the induction of LTP in a concentration-dependent manner. 3. The effect of 5-HT was blocked by the 5-HT1 receptor antagonist pindolol or the 5-HT2,7 receptor antagonist ritanserin, but not by the 5-HT3,4 receptor antagonist MDL72222. 4. These results suggest that 5-HT plays a role in suppressing the induction of LTP in the rat visual cortex.     

Linearity and normalization in simple cells of the macaque primary visual cortex

Simple cells in the primary visual cortex often appear to compute a weighted sum of the light intensity distribution of the visual stimuli that fall on their receptive fields. A linear model of these cells has the advantage of simplicity and captures a number of basic aspects of cell function. It, however, fails to account for important response nonlinearities, such as the decrease in response gain and latency observed at high contrasts and the effects of masking by stimuli that fail to elicit responses when presented alone. To account for these nonlinearities we have proposed a normalization model, which extends the linear model to include mutual shunting inhibition among a large number of cortical cells. Shunting inhibition is divisive, and its effect in the model is to normalize the linear responses by a measure of stimulus energy. To test this model we performed extracellular recordings of simple cells in the primary visual cortex of anesthetized macaques. We presented large stimulus sets consisting of (1) drifting gratings of various orientations and spatiotemporal frequencies; (2) plaids composed of two drifting gratings; and (3) gratings masked by full-screen spatiotemporal white noise. We derived expressions for the model predictions and fitted them to the physiological data. Our results support the normalization model, which accounts for both the linear and the nonlinear properties of the cells. An alternative model, in which the linear responses are subject to a compressive nonlinearity, did not perform nearly as well.     

Functional MRI reveals spatially specific attentional modulation in human primary visual cortex

Selective visual attention can strongly influence perceptual processing, even for apparently low-level visual stimuli. Although it is largely accepted that attention modulates neural activity in extrastriate visual cortex, the extent to which attention operates in the first cortical stage, striate visual cortex (area V1), remains controversial. Here, functional MRI was used at high field strength (3 T) to study humans during attentionally demanding visual discriminations. Similar, robust attentional modulations were observed in both striate and extrastriate cortical areas. Functional mapping of cortical retinotopy demonstrates that attentional modulations were spatially specific, enhancing responses to attended stimuli and suppressing responses when attention was directed elsewhere. The spatial pattern of modulation reveals a complex attentional window that is consistent with object-based attention but is inconsistent with a simple attentional spotlight. These data suggest that neural processing in V1 is not governed simply by sensory stimulation, but, like extrastriate regions, V1 can be strongly and specifically influenced by attention.     

Relationships between local synaptic connections and orientation domains in primary visual cortex

Combined optical imaging of ferret primary visual cortex in vivo and scanning laser photostimulation in brain slices were used to determine the spatial relationships between synaptic inputs onto individual neurons and the pattern of orientation columns. In the upper cortical layers, both excitatory and inhibitory inputs originated primarily from regions with orientation tuning similar to that of the recorded neurons; the shapes of the input tuning curves were indistinguishable. The orientation distributions of both types of inputs centered around the orientation of the recorded neurons, and no evidence for preferential cross-orientation inputs, either excitatory or inhibitory, was observed. These patterns of synaptic connectivity are most consistent with feedforward models for generation of orientation selectivity and are inconsistent with the patterns required by models based on cross-orientation inhibition.     

Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight

Neuronal responses were recorded from the striate cortex of monkeys trained to perform visual discrimination at locations in the visual field to which their attention was drawn. A subset of neurons showed vigorous responses to visual stimuli for trials in which the monkey was directing its attention to the respective receptive field location. In trials where attention is directed elsewhere, responses to the same stimuli were significantly reduced. In some cells the early response component was not modulated by attention, but later components were affected by the locus of attention. The results suggest the operation of a feedback in the paradigm that spotlights a topographically restricted area of V1 for further processing at higher levels.     

Contributions of individual layer 2-5 spiny neurons to local circuits in macaque primary visual cortex

We studied excitatory local circuits in the macaque primary visual cortex (VI) to investigate their relationships to the magnocellular (M) and parvocellular (P) streams. Sixty-two intracellularly labeled spiny neurons in layers 2-5 were analyzed. We made detailed observations of the laminar and columnar specificity of axonal arbors and noted correlations with dendritic arbors. We find evidence for considerable mixing of M and P streams by the local circuitry in VI. Such mixing is provided by neurons in the primary geniculate recipient layer 4C, as well as by neurons in both the supragranular and infragranular layers. We were also interested in possible differences in the axonal projections of neurons with different dendritic morphologies. We found that layer 4B spiny stellate and pyramidal neurons have similar axonal arbors. However, we identified two types of layer 5 pyramidal neuron. The majority have a conventional pyramidal dendritic morphology, a dense axonal arbor in layers 2.4B, and do not project to the white matter. Layer 5 projection neurons have an unusual "backbranching" dendritic morphology (apical dendritic branches arc downward rather than upward) and weak or no axonal arborization in layers 2-4B, but have long horizontal axonal projections in layer 5B. We find no strong projection from layer 5 pyramidal neurons to layer 6. In macaque V1 there appears to be no single source of strong local input to layer 6; only a minority of cells in layers 2-5 have axonal branches in layer 6 and these are sparse. Our results suggest that local circuits in V1 mediate interactions between M and P input that are complex and not easily incorporated into a simple framework.     

Parallel processing in the auditory cortex of primates

Evidence from anatomical tracer studies as well as lesions of the primary auditory cortex (AI) indicate that the principal relay nucleus of the auditory thalamus, the ventral part of the medial geniculate (MGv), projects in parallel to AI and the rostral area on the supratemporal plane of the macaque monkey. The caudomedial area, by contrast, receives input from MGv only indirectly via AI, and neurons in this area are often tuned to the spatial location of a complex sound. The belt areas on the lateral surface of the superior temporal gyrus receive input from the primary areas. Neurons in these areas respond better to more complex stimuli, such as band-pass noise pulses of frequency-modulated sweeps, than to pure tones. Often neurons in the lateral belt respond well to species-specific communication calls. The hypothesis is put forward that the central auditory pathways in the macaque monkey are organized into parallel streams, similar to the visual system, one for the processing of spatial information, the other for the processing of auditory "patterns". Evidence from neuroimaging studies in humans with MRI and PET are consistent with this hypothesis. Virtual auditory space stimuli lead to selective activation of an inferior parietal region, whereas speech-like stimuli activate superior temporal regions.     

Effects of stimulus integrality on visual attention in older and younger adults: a quantitative model-based analysis

Twenty-one older and 21 younger adults were administered a series of visual attention tasks. A series of quantitative models was applied to each observer's data to determine whether he or she performed optimally or suboptimally or showed a deficit-in-attentional processing. The results suggested that (a) older and younger observers were affected equally by the integrality-separability manipulation, (b) there are no age-related differences in selective attention performance for either integral or separable-dimension stimuli, (c) there are no age-related differences in dimensional integration performance with separable-dimension stimuli, and (d) older observers were more likely to be suboptimal when asked to integrate information from integral-dimension stimuli. Implications for current theories of attentional processing in normal aging are discussed.