Spatial distribution of contextual interactions in primary visual cortex and in visual perception

To examine the role of primary visual cortex in visuospatial integration, we studied the spatial arrangement of contextual interactions in the response properties of neurons in primary visual cortex of alert monkeys and in human perception. We found a spatial segregation of opposing contextual interactions. At the level of cortical neurons, excitatory interactions were located along the ends of receptive fields, while inhibitory interactions were strongest along the orthogonal axis. Parallel psychophysical studies in human observers showed opposing contextual interactions surrounding a target line with a similar spatial distribution. The results suggest that V1 neurons can participate in multiple perceptual processes via spatially segregated and functionally distinct components of their receptive fields.     

A morphological basis for orientation tuning in primary visual cortex

Feedforward connections are thought to be important in the generation of orientation-selective responses in visual cortex by establishing a bias in the sampling of information from regions of visual space that lie along a neuron's axis of preferred orientation. It remains unclear, however, which structural elements-dendrites or axons-are ultimately responsible for conveying this sampling bias. To explore this question, we have examined the spatial arrangement of feedforward axonal connections that link non-oriented neurons in layer 4 and orientation-selective neurons in layer 2/3 of visual cortex in the tree shrew. Target sites of labeled boutons in layer 2/3 resulting from focal injections of biocytin in layer 4 show an orientation-specific axial bias that is sufficient to confer orientation tuning to layer 2/3 neurons. We conclude that the anisotropic arrangement of axon terminals is the principal source of the orientation bias contributed by feedforward connections.     

Development of orientation tuning in simple cells of primary visual cortex

Orientation selectivity and its development are basic features of visual cortex. The original model of orientation selectivity proposes that elongated simple cell receptive fields are constructed from convergent input of an array of lateral geniculate nucleus neurons. However, orientation selectivity of simple cells in the visual cortex is generally greater than the linear contributions based on projections from spatial receptive field profiles. This implies that additional selectivity may arise from intracortical mechanisms. The hierarchical processing idea implies mainly linear connections, whereas cortical contributions are generally considered to be nonlinear. We have explored development of orientation selectivity in visual cortex with a focus on linear and nonlinear factors in a population of anesthetized 4-wk postnatal kittens and adult cats. Linear contributions are estimated from receptive field maps by which orientation tuning curves are generated and bandwidth is quantified. Nonlinear components are estimated as the magnitude of the power function relationship between responses measured from drifting sinusoidal gratings and those predicted from the spatial receptive field. Measured bandwidths for kittens are slightly larger than those in adults, whereas predicted bandwidths are substantially broader. These results suggest that relatively strong nonlinearities in early postnatal stages are substantially involved in the development of orientation tuning in visual cortex.     

GABA-mediated inhibition correlates with orientation selectivity in primary visual cortex of cat

Orientation selectivity is an important emergent property of neurons in the primary visual cortex, and inhibition is thought to play an important role in establishing this selectivity. But the relationship between strength of inhibition and orientation selectivity is unclear. To investigate this relationship, we electrophoretically applied the inhibitory transmitter GABA and the GABA(A) antagonist bicuculline on the same individual area 17 neurons in anesthetized cats. Neurons were classified as weakly orientation-selective, moderately orientation-selective, or strongly orientation-selective, according to the values of an orientation bias index. Orientation bias, half-width of the tuning curve at half-height and an orientation-specificity index (orthogonal to optimal ratio) were compared with or without GABA and bicuculline administration. GABA improved orientation selectivity with the greatest effects on weakly orientation-selective cells, smaller effects on moderately orientation-selective cells, and minimal effects on strongly orientation-selective cells; bicuculline diminished orientation selectivity the most on moderately and strongly orientation-selective cells, with minimal effects on weakly orientation-selective cells. We also found that orientation selectivity correlated with the level of neurons' spontaneous activity. These results suggest that the degree of orientation selectivity of an area 17 neuron correlates with its endogenous inhibition strength, and that GABAergic inhibition can bi-directionally regulate orientation selectivity. This correlation indicates that GABA-mediated inhibition plays an important role in establishing sharp orientation selectivity of individual neurons.     

Spatial frequency-specific contrast adaptation originates in the primary visual cortex

Adaptation to a high-contrast grating stimulus causes reduced sensitivity to subsequent presentation of a visual stimulus with similar spatial characteristics. This behavioral finding has been attributed by neurophysiological studies to processes within the visual cortex. However, some evidence indicates that contrast adaptation phenomena are also found in early visual pathways. Adaptation effects have been reported in retina and lateral geniculation nucleus (LGN). It is possible that these early pathways could be the physiological origin of the cortical adaptation effect. To study this, we recorded from single neurons in the cat's LGN. We find that contrast adaptation in the LGN, unlike that in the visual cortex, is not spatial frequency specific, i.e., adaptation effects apply to a broad range of spatial frequencies. In addition, aside from the amplitude attenuation, the shape of spatial frequency tuning curves of LGN cells is not affected by contrast adaptation. Again, these findings are unlike those found for cells in the visual cortex. Together, these results demonstrate that pattern specific contrast adaptation is a cortical process.     

Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex

Neurons in primary visual cortex are highly sensitive to the contrast, orientation, and temporal frequency of a visual stimulus. These three stimulus properties can be varied independently of one another, raising the question of how they interact to influence neuronal responses. We recorded from individual neurons in ferret primary visual cortex to determine the influence of stimulus contrast on orientation tuning, temporal-frequency tuning, and latency to visual response. Results show that orientation-tuning bandwidth is not affected by contrast level. Thus neurons in ferret visual cortex display contrast-invariant orientation tuning. Stimulus contrast does, however, influence the structure of orientation-tuning curves as measures of circular variance vary inversely with contrast for both simple and complex cells. This change in circular variance depends, in part, on a contrast-dependent change in the ratio of null to preferred orientation responses. Stimulus contrast also has an influence on the temporal-frequency tuning of cortical neurons. Both simple and complex cells display a contrast-dependent rightward shift in their temporal frequency-tuning curves that results in an increase in the highest temporal frequency needed to produce a half-maximum response (TF(50)). Results show that the degree of the contrast-dependent increase in TF(50) is similar for cortical neurons and neurons in the lateral geniculate nucleus (LGN) and indicate that subcortical mechanisms likely play a major role in establishing the degree of effect displayed by downstream neurons. Finally, results show that LGN and cortical neurons experience a contrast-dependent phase advance in their visual response. This phase advance is most pronounced for cortical neurons indicating a role for both subcortical and cortical mechanisms.     

Predicting the orientation of invisible stimuli from activity in human primary visual cortex

Humans can experience aftereffects from oriented stimuli that are not consciously perceived, suggesting that such stimuli receive cortical processing. Determining the physiological substrate of such effects has proven elusive owing to the low spatial resolution of conventional human neuroimaging techniques compared to the size of orientation columns in visual cortex. Here we show that even at conventional resolutions it is possible to use fMRI to obtain a direct measure of orientation-selective processing in V1. We found that many parts of V1 show subtle but reproducible biases to oriented stimuli, and that we could accumulate this information across the whole of V1 using multivariate pattern recognition. Using this information, we could then successfully predict which one of two oriented stimuli a participant was viewing, even when masking rendered that stimulus invisible. Our findings show that conventional fMRI can be used to reveal feature-selective processing in human cortex, even for invisible stimuli.     

Sparse coding in striate and extrastriate visual cortex

Theoretical studies of mammalian cortex argue that efficient neural codes should be sparse. However, theoretical and experimental studies have used different definitions of the term "sparse" leading to three assumptions about the nature of sparse codes. First, codes that have high lifetime sparseness require few action potentials. Second, lifetime-sparse codes are also population-sparse. Third, neural codes are optimized to maximize lifetime sparseness. Here, we examine these assumptions in detail and test their validity in primate visual cortex. We show that lifetime and population sparseness are not necessarily correlated and that a code may have high lifetime sparseness regardless of how many action potentials it uses. We measure lifetime sparseness during presentation of natural images in three areas of macaque visual cortex, V1, V2, and V4. We find that lifetime sparseness does not increase across the visual hierarchy. This suggests that the neural code is not simply optimized to maximize lifetime sparseness. We also find that firing rates during a challenging visual task are higher than theoretical values based on metabolic limits and that responses in V1, V2, and V4 are well-described by exponential distributions. These findings are consistent with the hypothesis that neurons are optimized to maximize information transmission subject to metabolic constraints on mean firing rate.     

Spatial structure and symmetry of simple-cell receptive fields in macaque primary visual cortex

I present measurements of the spatial structure of simple-cell receptive fields in macaque primary visual cortex (area V1). Similar to previous findings in cat area 17, the spatial profile of simple-cell receptive fields in the macaque is well described by two-dimensional Gabor functions. A population analysis reveals that the distribution of spatial profiles in primary visual cortex lies approximately on a one-parameter family of filter shapes. Surprisingly, the receptive fields cluster into even- and odd-symmetry classes with a tendency for neurons that are well tuned in orientation and spatial frequency to have odd-symmetric receptive fields. The filter shapes predicted by two recent theories of simple-cell receptive field function, independent component analysis and sparse coding, are compared with the data. Both theories predict receptive fields with a larger number of subfields than observed in the experimental data. In addition, these theories do not generate receptive fields that are broadly tuned in orientation and low-pass in spatial frequency, which are commonly seen in monkey V1. The implications of these results for our understanding of image coding and representation in primary visual cortex are discussed.     

Temporal coding of contrast in primary visual cortex: when, what, and why

How do neurons in the primary visual cortex (V1) encode the contrast of a visual stimulus? In this paper, the information that V1 responses convey about the contrast of static visual stimuli is explicitly calculated. These responses often contain several easily distinguished temporal components, which will be called latency, transient, tonic, and off. Calculating the information about contrast conveyed in each component and in groups of components makes it possible to delineate aspects of the temporal structure that may be relevant for contrast encoding. The results indicate that as much or more contrast-related information is encoded into the temporal structure of spike train responses as into the firing rate and that the temporally coded information is manifested most strongly in the latency to response onset. Transient, tonic, and off responses contribute relatively little. The results also reveal that temporal coding is important for distinguishing subtle contrast differences, whereas firing rates are useful for gross discrimination. This suggests that the temporal structure of neurons' responses may extend the dynamic range for contrast encoding in the primate visual system.     

Long adaptation reveals mostly attractive shifts of orientation tuning in cat primary visual cortex

In the adult brain, sensory cortical neurons undergo transient changes of their response properties following prolonged exposure to an appropriate stimulus (adaptation). In cat V1, orientation-selective cells shift their preferred orientation after being adapted to a non-preferred orientation. There are conflicting reports as to the direction of those shifts, towards (attractive) or away (repulsive) from the adapter. Moreover, the mechanisms underlying attractive shifts remain unexplained. In the present investigation we show that attractive shifts are the most frequent outcome of a 12 min adaptation. Overall, cells displaying selectivity for oblique orientations exhibit significantly larger shifts than cells tuned to cardinal orientations. In addition, cells selective to cardinal orientations had larger shift amplitudes when the absolute difference between the original preferred orientation and the adapting orientation increased. Conversely, cells tuned to oblique orientations exhibited larger shift amplitudes when this absolute orientation difference was narrower. Hence, neurons tuned to oblique contours appear to show more plasticity in response to small perturbations. Two different mechanisms appear to produce attractive and repulsive orientation shifts. Attractive shifts result from concurrent response depression on the non-adapted flank and selective response facilitation on the adapted flank of the orientation tuning curve. In contrast, repulsive shifts are caused solely by response depression on the adapted flank. We suggest that an early mechanism leads to repulsive shifts while attractive shifts engage a subsequent late facilitation. A potential role for attractive shifts may be improved stimulus discrimination around the adapting orientation.     

Retinal origin of orientation maps in visual cortex

The orientation map is a hallmark of primary visual cortex in higher mammals. It is not yet known how orientation maps develop, what function they have in visual processing and why some species lack them. Here we advance the notion that quasi-periodic orientation maps are established by moiré interference of regularly spaced ON- and OFF-center retinal ganglion cell mosaics. A key prediction of the theory is that the centers of iso-orientation domains must be arranged in a hexagonal lattice on the cortical surface. Here we show that such a pattern is observed in individuals of four different species: monkeys, cats, tree shrews and ferrets. The proposed mechanism explains how orientation maps can develop without requiring precise patterns of spontaneous activity or molecular guidance. Further, it offers a possible account for the emergence of orientation tuning in single neurons despite the absence of orderly orientation maps in rodents species.     

Contrast invariance of orientation tuning in cat primary visual cortex neurons depends on stimulus size

Key points

• The process of orientation tuning is an important and well‐characterized feature of neurons in primary visual cortex.
• The combination of ascending and descending circuits involved is not only relevant to understanding visual processing but the function of neocortex in general.
• The classic feed‐forward model of orientation tuning predicts a broadening effect due to increasing contrast; yet, experimental results consistently report contrast invariance.
• We show here that contrast invariance actually depends on stimulus size such that large stimuli extending beyond the neuron''s receptive field engage circuits that promote invariance, whereas optimally sized, smaller stimuli result in contrast variance that is more in line with the classical orientation tuning model.
• These results illustrate the importance of optimizing stimulus parameters to best reflect the sensory pathways under study and provide new clues about different circuits that may be involved in variant and invariant response properties.

Abstract

Selective response to stimulus orientation is a key feature of neurons in primary visual cortex, yet the underlying mechanisms generating orientation tuning are not fully understood. The combination of feed‐forward and cortical mechanisms involved is not only relevant to understanding visual processing but the function of neocortex in general. The classic feed‐forward model predicts that orientation tuning should broaden considerably with increasing contrast; however, experimental results consistently report contrast invariance. We show here, in primary visual cortex of anaesthetized cats under neuromuscular blockade, that contrast invariance occurs when visual stimuli are large enough to include the extraclassical surround (ECS), which is likely to involve circuits of suppression that may not be entirely feed‐forward in origin. On the other hand, when stimulus size is optimized to the classical receptive field of each neuron, the population average shows a statistically significant 40% increase in tuning width at high contrast, demonstrating that contrast variance of orientation tuning can occur. Conversely, our results also suggest that the phenomenon of contrast invariance relies in part on the presence of the ECS. Moreover, these results illustrate the importance of optimizing stimulus parameters to best reflect the neural pathways under study.

Abbreviations

CRF

classical receptive field

CV

circular variance

ECS

extraclassical receptive field

HWHH

half‐width at half‐height

LGN

lateral geniculate nucleus

V1

primary visual cortex

     

Influence of adapting speed on speed and contrast coding in the primary visual cortex of the cat

Adaptation is a ubiquitous property of the visual system. Adaptation often improves the ability to discriminate between stimuli and increases the operating range of the system, but is also associated with a reduced ability to veridically code stimulus attributes. Adaptation to luminance levels, contrast, orientation, direction and spatial frequency has been studied extensively, but knowledge about adaptation to image speed is less well understood. Here we examined how the speed tuning of neurons in cat primary visual cortex was altered after adaptation to speeds that were slow, optimal, or fast relative to each neuron's speed response function. We found that the preferred speed (defined as the speed eliciting the peak firing rate) of the neurons following adaptation was dependent on the speed at which they were adapted. At the population level cells showed decreases in preferred speed following adaptation to speeds at or above the non-adapted speed, but the preferred speed did not change following adaptation to speeds lower than the non-adapted peak. Almost all cells showed response gain control (reductions in absolute firing capacity) following speed adaptation. We also investigated the speed dependence of contrast adaptation and found that most cells showed contrast gain control (rightward shifts of their contrast response functions) and response gain control following adaptation at any speed. We conclude that contrast adaptation may produce the response gain control associated with speed adaptation, but shifts in preferred speed require an additional level of processing beyond contrast adaptation. A simple model is presented that is able to capture most of the findings.     

Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects

A fundamental feature of neural circuitry in the primary visual cortex (V1) is the existence of recurrent excitatory connections between spiny neurons, recurrent inhibitory connections between smooth neurons, and local connections between excitatory and inhibitory neurons. We modeled the dynamic behavior of intermixed excitatory and inhibitory populations of cells in V1 that receive input from the classical receptive field (the receptive field center) through feedforward thalamocortical afferents, as well as input from outside the classical receptive field (the receptive field surround) via long-range intracortical connections. A counterintuitive result is that the response of oriented cells can be facilitated beyond optimal levels when the surround stimulus is cross-oriented with respect to the center and suppressed when the surround stimulus is iso-oriented. This effect is primarily due to changes in recurrent inhibition within a local circuit. Cross-oriented surround stimulation leads to a reduction of presynaptic inhibition and a supraoptimal response, whereas iso-oriented surround stimulation has the opposite effect. This mechanism is used to explain the orientation and contrast dependence of contextual interactions in primary visual cortex: responses to a center stimulus can be both strongly suppressed and supraoptimally facilitated as a function of surround orientation, and these effects diminish as stimulus contrast decreases.     

Laminar processing of stimulus orientation in cat visual cortex

One of the most salient features to emerge in visual cortex is sensitivity to stimulus orientation. Here we asked if orientation selectivity, once established, is altered by successive stages of cortical processing. We measured patterns of orientation selectivity at all depths of the cat's visual cortex by making whole-cell recordings with dye-filled electrodes. Our results show that the synaptic representation of orientation indeed changes with position in the microcircuit, as information passes from layer 4 to layer 2+3 to layer 5. At the earliest cortical stage, for simple cells in layer 4, orientation tuning curves for excitation (depolarization) and inhibition (hyperpolarization) had similar peaks (within 0–7 deg,   n = 11  ) and bandwidths. Further, the sharpness of orientation selectivity covaried with receptive field geometry (   r = 0.74  ) - the more elongated the strongest subregion, the shaper the tuning. Tuning curves for complex cells in layer 2+3 also had similar peaks (within 0–4 deg,   n = 7  ) and bandwidths. By contrast, at a later station, layer 5, the preferred orientation for excitation and inhibition diverged such that the peaks of the tuning curves could be as far as 90 deg apart (average separation, 54 deg;   n = 6  ). Our results support the growing consensus that orientation selectivity is generated at the earliest cortical level and structured similarly for excitation and inhibition. Moreover, our novel finding that the relative tuning of excitation and inhibition changes with laminar position helps resolve prior controversy about orientation selectivity at later phases of processing and gives a mechanistic view of how the cortical circuitry recodes orientation.     

Spatial distribution of inhibitory synaptic connections during development of ferret primary visual cortex

Intracortical inhibition in the primary visual cortex plays an important role in creating properties like orientation and direction selectivity. However, the development of the spatial pattern of inhibitory connections is largely unexplored. This was investigated in the present study. Tangential slices of layers 2/3 of ferret striate cortex were prepared for whole-cell patch clamp recordings, and presynaptic inhibitory inputs to pyramidal neurons were scanned by local photolysis of Nmoc-caged glutamate. Inhibitory synaptic currents (IPSCs) were first detected around postnatal day (P) 17. They originated locally around the recorded cells. Both the number and the total areas supplying the inhibitory inputs increased thereafter and peaked at the time around and shortly after eye opening (P29–37). A refinement period then followed in which the areas providing the majority of inhibitory inputs shrank from 600 µm around the recorded neurons to 200–300 µm in more mature animals (P38). The amplitude of IPSCs increased progressively with increasing age. Long-range inhibitory inputs (>600 µm) were present around eye opening and they often developed into a clustered patchy pattern in more mature animals (P38). In summary, our results show a refinement and clustering in the spatial pattern of inhibitory connections during postnatal development of ferret visual cortex.     

Formal and attribute-specific information in primary visual cortex

We estimate the rates at which neurons in the primary visual cortex (V1) of anesthetized macaque monkeys transmit stimulus-related information in response to three types of visual stimulus. The stimuli-randomly modulated checkerboard patterns, stationary sinusoidal gratings, and drifting sinusoidal gratings-have very different spatiotemporal structures. We obtain the overall rate of information transmission, which we call formal information, by a direct method. We find the highest information rates in the responses of simple cells to drifting gratings (median: 10.3 bits/s, 0.92 bits/spike); responses to randomly modulated stimuli and stationary gratings transmit information at significantly lower rates. In general, simple cells transmit information at higher rates, and over a larger range, than do complex cells. Thus in the responses of V1 neurons, stimuli that are rapidly modulated do not necessarily evoke higher information rates, as might be the case with motion-sensitive neurons in area MT. By an extension of the direct method, we parse the formal information into attribute-specific components, which provide estimates of the information transmitted about contrast and spatiotemporal pattern. We find that contrast-specific information rates vary across neurons-about 0.3 to 2.1 bits/s or 0.05 to 0.22 bits/spike-but depend little on stimulus type. Spatiotemporal pattern-specific information rates, however, depend strongly on the type of stimulus and neuron (simple or complex). The remaining information rate, typically between 10 and 32% of the formal information rate for each neuron, cannot be unambiguously assigned to either contrast or spatiotemporal pattern. This indicates that some information concerning these two stimulus attributes is confounded in the responses of single neurons in V1. A model that considers a simple cell to consist of a linear spatiotemporal filter followed by a static rectifier predicts higher information rates than are found in real neurons and completely fails to replicate the performance of real cells in generating the confounded information.     

Neural coding of global form in the human visual cortex

Extensive psychophysical and computational work proposes that the perception of coherent and meaningful structures in natural images relies on neural processes that convert information about local edges in primary visual cortex to complex object features represented in the temporal cortex. However, the neural basis of these mid-level vision mechanisms in the human brain remains largely unknown. Here, we examine functional MRI (fMRI) selectivity for global forms in the human visual pathways using sensitive multivariate analysis methods that take advantage of information across brain activation patterns. We use Glass patterns, parametrically varying the perceived global form (concentric, radial, translational) while ensuring that the local statistics remain similar. Our findings show a continuum of integration processes that convert selectivity for local signals (orientation, position) in early visual areas to selectivity for global form structure in higher occipitotemporal areas. Interestingly, higher occipitotemporal areas discern differences in global form structure rather than low-level stimulus properties with higher accuracy than early visual areas while relying on information from smaller but more selective neural populations (smaller voxel pattern size), consistent with global pooling mechanisms of local orientation signals. These findings suggest that the human visual system uses a code of increasing efficiency across stages of analysis that is critical for the successful detection and recognition of objects in complex environments.