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Models of orientation and ocular dominance columns in the visual cortex: a critical comparison.

Orientation and ocular dominance maps in the primary visual cortex of mammals are among the most thoroughly investigated of the patterns in the cerebral cortex. A considerable amount of work has been dedicated to unraveling both their detailed structure and the neural mechanisms that underlie their formation and development. Many schemes have been proposed, some of which are in competition. Some models focus on development of receptive fields while others focus on the structure of cortical maps, i.e., the arrangement of receptive field properties across the cortex. Each model used different means to determine its success at reproducing experimental map patterns, often relying principally on visual comparison. Experimental data are becoming available that allow a more careful evaluation of models. In this contribution more than 10 of the most prominent models of cortical map formation and structure are critically evaluated and compared with the most recent experimental findings from macaque striate cortex. Comparisons are based on properties of the predicted or measured cortical map patterns. We introduce several new measures for comparing experimental and model map data that reveal important differences between models. We expect that the use of these measures will improve current models by helping determine parameters to match model maps to experimental data now becoming available from a variety of species. Our study reveals that (1) despite apparent differences, many models are based on similar principles and consequently make similar predictions, (2) several models produce orientation map patterns that are not consistent with the experimental data from macaques, regardless of the plausibility of the models' suggested physiological implementations, and (3) no models have yet fully accounted for both the local and the global relationships between orientation and ocular dominance map patterns.

Animals↗

Retinotopic organization of human visual cortex mapped with positron-emission tomography.

The retinotopic organization of primary visual cortex was mapped in normal human volunteers. Positron-emission tomographic measurements of regional cerebral blood flow were employed to detect focal functional brain activation. Oxygen-15-labeled water, delivered by intravenous bolus, was used as the blood flow tracer to allow multiple stimulated-state (n = 5) and control-state (n = 3) measurements to be acquired for each of 7 subjects. Responses were identified by applying a maximum-detection algorithm to subtraction-format images of the stimulus-induced change in cerebral blood flow. Response locales were described using a standardized system of stereotactic coordinates. Changes in stimulus location (macular, perimacular, peripheral, upper-field, lower-field) caused systematic, highly significant changes in response locale within visual cortex. Discrete extrastriate visual responses were also observed.

Adult↗

Postnatal development of binocular disparity sensitivity in neurons of the primate visual cortex.

In macaque monkeys, the age at which neurons in the primary visual cortex (V1) become sensitive to interocular image disparities, a prerequisite for stereopsis, is a matter of conjecture. To resolve this fundamental issue in binocular vision development, we measured the responsiveness of individual V1 neurons in anesthetized and paralyzed infant monkeys as a function of the relative, interocular, spatial phase of dichoptic sine-wave gratings. We found that an adult-like proportion of units were sensitive to interocular image disparity as early as the sixth postnatal day, several weeks before the onset age for stereopsis in monkeys. The ocular dominance distributions of cells in infant monkeys were also indistinguishable from those of adults. Thus, at or only a few days after birth, V1 neurons are capable of combining neural signals from the two eyes as in adults and are sensitive to interocular image disparities. However, the monocular spatial-frequency response properties of these disparity-sensitive units were immature, and their overall responsiveness was far lower than that in adults. During the first 4 postnatal weeks, both the spatial frequency response properties and the peak response amplitude rapidly improved, which resulted in a corresponding increase in the absolute sensitivity of individual units to interocular disparity. The results demonstrate that early binocular vision development in monkeys is not constrained by a paucity of disparity-sensitive V1 neurons but, instead, by the relative immaturity of the spatial response properties and the overall unresponsiveness of existing disparity-sensitive neurons.

Animals↗

Two-dimensional analysis of the spacing of ocular dominance columns in normally raised and strabismic kittens.

In the primary visual cortex of cats, ferrets and macaque monkeys, the thalamocortical afferents conveying signals from the two eyes terminate in alternating regions of layer IV known as ocular dominance columns. Previous experiments have indicated that the periodicity of these columns can be influenced by visual experience: compared to normally raised animals both strabismic cats and cats raised with alternating monocular exposure displayed an increased spacing of adjacent ocular dominance columns in the primary visual cortex (area 17). However, recently it was shown that the formation of ocular dominance columns begins much earlier than previously supposed, indicating that early visual experience might only have a limited influence on the development of the spatial pattern of ocular dominance columns. We therefore visualized the complete pattern of ocular dominance columns in area 17 of normally raised and strabismic kittens during early postnatal development (age 3-6 weeks), particularly focussing on littermates. In addition, we used a previously developed spatial analysis (period statistics) to quantify columnar spacing two-dimensionally. We observed a pronounced interindividual variability in both normally raised and strabismic animals, with column spacings ranging from 783 to 1362 microm. In contrast to previous reports, there were no significant differences in columnar periodicity between normally raised and strabismic cats. These data indicate that rearing has less influence on column spacing while the interindividual variability is much greater than previously supposed, suggesting that genetic differences have an influence on column spacing.

Animals↗

Disparity detection in anticorrelated stereograms.

Recent physiological observations in which stimuli with opposite contrast signs in the two eyes have been used (anticorrelated stereograms) show that these stimuli evoke responses in primary visual cortex which are the reverse of responses to correlated stimuli. Psychophysical investigations reveal no such reversals: reversed-contrast bars with crossed disparities are seen in front of those with uncrossed disparities. For anticorrelated random-dot stereograms human subjects perceive no depth at all, except at low dot densities. However, these human studies were carried out with stimuli that differed in several ways from those used in physiological studies. We therefore reexamined psychophysical responses using stimuli similar to those used for physiological recordings. Our results confirm the previous findings: there is no evidence of a reversed depth sensation for bar stereograms (crossed disparities are never seen behind uncrossed disparities), and subjects are unable to detect depth in anticorrelated random-dot stereograms at the densities used for the physiological recordings. The discrepancy between the psychophysical data and the responses of single neurons in primary visual cortex suggests that further processing outside area V1 is necessary to provide the signals that produce the sensation of stereoscopic depth.

Computer Graphics↗

Molecular cloning and differential expression of the cat immediate early gene c-fos.

Recently, the effect of binocular central retinal lesions on the expression of immediate early genes in the visual system of adult cats was demonstrated using in situ hybridization and immunocytochemistry. The present study was undertaken to quantify cat c-fos mRNA expression differences in the cat primary visual cortex after sensory deafferentation. Prior to quantification, DNA fragments obtained using reverse transcription-polymerase chain reaction (RT-PCR) in combination with rapid amplification of complementary DNA ends (RACE) were cloned and sequenced. This provided us with the necessary sequence(1) information to prepare cat-specific c-fos primers for the development of a new quantitative RT-PCR assay. We optimized a reverse transcription-competitive polymerase chain reaction (RT-cPCR) method with a heterologous DNA fragment (competitor) as external standard to quantify relative amounts of cat c-fos mRNA expression levels. Internal standardization was accomplished by quantifying, in a parallel RT-cPCR, a well-characterized housekeeping gene, glyceraldehyde-3-phosphate dehydrogenase (GAPDH). This cat-specific RT-cPCR assay allowed us to measure c-fos mRNA expression levels in central and peripheral regions of primary visual cortex in normal and retinal lesion cats.

Amino Acid Sequence↗

In vivo 31P magnetic resonance spectroscopy of human brain at 7 T: an initial experience.

In vivo (31)P spectra were acquired from the human primary visual cortex at 7 T. The relaxation times of the cerebral metabolites, intracellular pH, rate constant (k(f)) of the creatine kinase (CK) reaction, and nuclear Overhauser enhancement (NOE) on the detected phosphorus moieties from irradiation of the water spins were measured from normal subjects. With a 5-cm-diameter surface coil, 3D (31)P chemical shift imaging was performed with a spatial resolution of 7.5 ml and an acquisition resolution of 8 min, resulting in a signal-to-noise ratio (SNR) for phosphocreatine (PCr) resonance of 32. The apparent T(1) and T(2) of PCr measured at 7 T were 3.37 +/- 0.29 s and 132.0 +/- 12.8 ms, respectively, which were considerably longer than those of adenosine triphosphate (ATP) (T(1): 1.02-1.27 s; T(2): 25-26 ms). The NOE measured in this study was 24.3% +/- 1.6% for PCr, and 10% for ATP. The k(f) measured in the human primary visual cortex was 0.24 +/- 0.03 s(-1). The results from this study suggest that ultra-high-field strength is advantageous for performing in vivo (31)P magnetic resonance spectroscopy (MRS) in the human brain.

Adenosine Triphosphate↗

Orientation tuning and synchronization in the hypercolumn model.

The orientation selectivity in the firing rate of neurons is one of the most well-known properties of neurons in the primary visual cortex. To understand the dynamical mechanism of the orientation tuning, we introduce a biologically plausible network for a hypercolumn and investigate dynamical responses of its columnar activities. Numerical simulations show that the spike activities between excitatory cells in the same column exhibit strong synchronization and sharp orientation selectivity. The tuning curves for the synchronized activities also show orientation selectivity similar to those for the firing rate. The comparison between the two tuning curves for the firing rate and the synchronized activities suggests that the orientation selectivity is strongly correlated with the synchronized activities. We find from the analysis of columnar activities that the orientation selectivity depends strongly upon the inhibitory coupling strength and the synchronization upon the excitatory coupling strength. In particular, we find that at appropriate coupling parameters both sharp orientation selectivity and maximal synchronization can be achieved. This suggests the importance of the balance between the excitatory coupling and the inhibitory coupling in the primary visual cortex for visual information processing.

Action Potentials↗

Structure and function of parallel pathways in the primate early visual system.

Parallel processing streams in the primate visual system originate from more than a dozen anatomically and functionally distinct types of retinal ganglion cells (RGCs). A central problem in determining how visual information is processed is understanding how each of these RGC types connects to more central structures, including the lateral geniculate nucleus (LGN) of the thalamus and (via the LGN) the primary visual cortex. Nevertheless, the available functional and anatomical evidence linking together specific cell types across these structures is surprisingly indirect. This review evaluates the available evidence and assesses the strength of the many inferences that can be made from these observations. There is strong evidence that parasol RGCs are the provenance of the magnocellular (M) visual pathway and that midget RGCs give rise to the parvocellular (P) pathway. Furthermore, the M and P pathways remain segregated up to the input layer of primary visual cortex. The relationships between the numerous other RGC types and cell types in the LGN remain less certain. and there remains ambiguity about how best to define additional pathways, such as the koniocellular (K) pathway, which probably arise from these other, less common, RGC types.

Action Potentials↗

Learning the invariance properties of complex cells from their responses to natural stimuli.

Neurons in primary visual cortex are typically classified as either simple or complex. Whereas simple cells respond strongly to grating and bar stimuli displayed at a certain phase and visual field location, complex cell responses are insensitive to small translations of the stimulus within the receptive field [Hubel & Wiesel (1962) J. Physiol. (Lond.), 160, 106-154; Kjaer et al. (1997) J. Neurophysiol., 78, 3187-3197]. This constancy in the response to variations of the stimuli is commonly called invariance. Hubel and Wiesel's classical model of the primary visual cortex proposes a connectivity scheme which successfully describes simple and complex cell response properties. However, the question as to how this connectivity arises during normal development is left open. Based on their work and inspired by recent physiological findings we suggest a network model capable of learning from natural stimuli and developing receptive field properties which match those of cortical simple and complex cells. Stimuli are drawn from videos obtained by a camera mounted to a cat's head, so they should approximate the natural input to the cat's visual system. The network uses a competitive scheme to learn simple and complex cell response properties. Employing delayed signals to learn connections between simple and complex cells enables the model to utilize temporal properties of the input. We show that the temporal structure of the input gives rise to the emergence and refinement of complex cell receptive fields, whereas removing temporal continuity prevents this processes. This model lends a physiologically based explanation of the development of complex cell invariance response properties.

Animals↗

Visual function in the brain-damaged child.

The essential role of the primary visual cortex in visual processing has been extensively studied over the last century or more. Injuries to the visual cortex in adult humans can produce blindness, referred to as "cortical blindness". In children some degree of visual recovery has been noted in comparable injuries and for that reason the term "cortical visual impairment" has been suggested as a more appropriate diagnosis in children. This term is, however, inaccurate as a significant number of children with visual loss and neurologic damage have injuries to the noncerebral pathways (for example--optic radiations in children with periventricular leukomalacia). In this study we compare visual outcomes and recovery in children with primary visual cortex lesions vs those with periventricular leukomalacia. We suggest that the poorer outcomes of children with periventricular leukomalacia could have been predicted based on studies of the mechanisms of visual recovery in infant animals following visual cortex ablation.

Blindness, Cortical↗

Cooperative and competitive spatial interactions in motion integration.

Recovering the velocity of objects moving in the visual field requires both the integration and segmentation of local neuronal responses elicited by moving stimuli in primary visual cortex. Herein, we investigate the effects of the contrast, density, spatial proximity, spatial frequency, and spatial configuration of component motions on these complementary processes. Measuring the ability of human observers to discriminate the global direction of motion displays composed of spatially distributed patches of drifting gratings whose motion is locally ambiguous, we provide psychophysical evidence that linking component motion across space is facilitated at low contrast and high patch density. Furthermore, direction discrimination depends on the spatial frequency of component gratings and is more accurate for spatial configurations that contain "virtual" L junctions as compared to configurations composed of "virtual" T junctions. We suggest that the conditions yielding global motion coherence can be accounted for by the existence of anisotropic cooperative/competitive, contrast-dependent, long-range interactions among oriented direction-selective units. In addition, we bring evidence that motion segmentation processes rely upon the processing of moving local spatial discontinuities. The results are discussed in the light of recent psychophysical and physiological evidence that long-range excitatory and inhibitory interactions within primary visual cortex modulate perceptual linking.

Contrast Sensitivity↗

A multichip aVLSI system emulating orientation selectivity of primary visual cortical cells.

In this paper, we designed and fabricated a multichip neuromorphic analog very large scale integrated (aVLSI) system, which emulates the orientation selective response of the simple cell in the primary visual cortex. The system consists of a silicon retina and an orientation chip. An image, which is filtered by a concentric center-surround (CS) antagonistic receptive field of the silicon retina, is transferred to the orientation chip. The image transfer from the silicon retina to the orientation chip is carried out with analog signals. The orientation chip selectively aggregates multiple pixels of the silicon retina, mimicking the feedforward model proposed by Hubel and Wiesel. The chip provides the orientation-selective (OS) outputs which are tuned to 0 degrees, 60 degrees, and 120 degrees. The feed-forward aggregation reduces the fixed pattern noise that is due to the mismatch of the transistors in the orientation chip. The spatial properties of the orientation selective response were examined in terms of the adjustable parameters of the chip, i.e., the number of aggregated pixels and size of the receptive field of the silicon retina. The multichip aVLSI architecture used in the present study can be applied to implement higher order cells such as the complex cell of the primary visual cortex.

Action Potentials↗

The disinhibitory zone of the striate neuron receptive field and its sensitivity to cross-like figures.

Acute experiments on immobilized anesthetized cats were used to confirm the suggestion that the sensitivity of many neurons on the primary visual cortex to cross-shaped, angular, and Y-shaped figures may be determined by the presence within their receptive fields of disinhibitory zones, which block end-stopping inhibition. A total of 55 neurons (84 functions, i.e.. on and off responses) were used for studies of sensitivity to crosses, and responses to single bars of different lengths were compared before and after stimulation of an additional lateral zone of the field (the presumptive disinhibitory zone), which was located in terms of responses to crosses. Seventeen of the 55 cells in which increases in the length of a single bar decreased responses, i.e., which demonstrated end-stopping inhibition, showed significant increases in responses (by an average factor of 2.06 +/- 0.16) during simultaneous stimulation of the lateral zone of the receptive field, which we interpreted as a disinhibitory effect on end-stopping inhibition. These data provide the first direct evidence for the role of end-stopping inhibition and its blockade by the disinhibitory zone of the receptive field in determining the sensitivity of some neurons in the primary visual cortex of the cat to cross-shaped figures.

Animals↗

Geometry and the visual brain.

Receptive fields structure of neurons in primary visual cortex suggests that they process visual stimuli in the frequency domain, in a way similar to the frequency analysis performed in the auditory system. As a consequence, both psychophysicists and electrophysiologists have long probed the visual system using extended sine wave gratings that are well localized in the frequency domain but poorly defined in visual space. Meanwhile, how the brain processes the geometrical properties and the spatial and temporal relationships between stimulus parts has received less attention. Recent progress in visual neuroscience that uncovered long-range horizontal connections between cortical neurons and revealed the complex architecture of primary visual cortex and feedback connectivity led to new insights concerned with the processing of geometrical properties of visual stimuli in V1. This paper presents a short historical perspective of the emergence of new issues related to the cortical architecture and its functional consequences on the processing of geometrical properties.

Animals↗

Functional imaging of visuospatial processing in Alzheimer's disease.

Alzheimer's disease (AD) is known to cause a variety of disturbances of higher visual functions that are closely related to the neuropathological changes. Visual association areas are more affected than primary visual cortex. Additionally, there is evidence from neuropsychological and imaging studies during rest or passive visual stimulation that the occipitotemporal pathway is less affected than the parietal pathway. Our goal was to investigate functional activation patterns during active visuospatial processing in AD patients and the impact of local cerebral atrophy on the strength of functional activation. Fourteen AD patients and fourteen age-matched controls were measured with functional magnetic resonance imaging (fMRI) while they performed an angle discrimination task. Both groups revealed overlapping networks engaged in angle discrimination including the superior parietal lobule (SPL), frontal and occipitotemporal (OTC) cortical regions, primary visual cortex, basal ganglia, and thalamus. The most pronounced differences between the two groups were found in the SPL (more activity in controls) and OTC (more activity in patients). The differences in functional activation between the AD patients and controls were partly explained by the differences in individual SPL atrophy. These results indicate that parietal dysfunction in mild to moderate AD is compensated by recruitment of the ventral visual pathway. We furthermore suggest that local cerebral atrophy should be considered as a covariate in functional imaging studies of neurodegenerative disorders.

Aged↗

Attentional effects in the visual pathways: a whole-brain PET study.

Attentional effects in the visual pathways were investigated by contrasting the distribution of regional cerebral blood flow (rCBF) measured by H(2)(15)O positron emission tomography (PET) during performance of a shape-matching task with the distribution of rCBF during a less demanding color-matching task. The two tasks were performed using the same stimuli: pairs of colored random shapes shown at a fixed rate (2 s per pair). In the shape-matching task, the subjects determined whether the two stimuli were the same in shape regardless of differences in size or color. In the color-matching task, the subjects determined whether the two stimuli were the same in color regardless of differences in size or shape. Mean reaction time for shape-matching exceeded mean reaction time for color-matching by nearly 200 ms. The corresponding shape-color comparison showed extensive bilateral increases in rCBF in visual areas in the occipital and parietal lobes, including the primary visual cortex. Subcortical activations were found in cerebellum (particularly the vermis) and in the thalamus with the focus in a region comprising the lateral geniculate nucleus, the pulvinar, and adjacent parts of the reticular nucleus. Frontal activations were found in a region that seems implicated in visual short-term memory (posterior parts of the superior sulcus and the middle gyrus). The reverse, color-shape comparison showed bilateral increases in rCBF in the anterior cingulate gyri, superior frontal gyri, and superior and middle temporal gyri. The attentional effects found by the shape-color comparison in the thalamus and the primary visual cortex may have been generated by feedback signals preserving visual representations of selected stimuli in short-term memory.

Adult↗

Parvalbumin and calbindin D-28k immunoreactivities coexist within cytochrome oxidase-rich compartments of squirrel monkey area 18.

Previous studies have demonstrated the presence of the calcium-binding proteins parvalbumin (PARV) and calbindin D-28k (CALB) in interdigitating neuronal systems of the primary visual cortex of primates (Celio et al. 1986; Hendry et al. 1989; Van Brederode et al. 1990). Since the processing of visual information takes place in the higher cortical areas (Hubel 1982), we wondered if complementarity of expression is maintained in the secondary visual cortex (area 18). We therefore examined tangential and coronal sections from the occipital lobe of squirrel monkeys using immunohistochemical techniques employing polyclonal antibodies against PARV and CALB. The pattern of PARV immunoreactivity is characterized by tangentially organized, alternating thick and thin stripes, separated by areas of lower immunoreactivity. Both the thick and thin stripes consist of PARV-immunoreactive neuropil. CALB immunoreactivity forms mainly thick stripes containing large numbers of labelled neurons. Thus in area 18, these zones of increased immunoreactivity coincide with the compartments revealing increased cytochrome oxidase activity, whereas the distribution of PARV and CALB is almost complementary in the subcortical visual centre and in the primary visual cortex (area 17) of New World monkeys.

Animals↗