A Postnatal Critical Period for Orientation Plasticity in the Cat Visual Cortex

Orientation selectivity of primary visual cortical neurons is an important requisite for shape perception. Although numerous studies have been previously devoted to a question of how orientation selectivity is established and elaborated in early life, how the susceptibility of orientation plasticity to visual experience changes in time remains unclear. In the present study, we showed a postnatal sensitive period profile for the modifiability of orientation selectivity in the visual cortex of kittens reared with head-mounted goggles for stable single-orientation exposure. When goggle rearing (GR) started at P16-P30, 2 weeks of GR induced a marked over-representation of the exposed orientation, and 2 more weeks of GR consolidated the altered orientation maps. GR that started later than P50, in turn, induced the under-representation of the exposed orientation. Orientation plasticity in the most sensitive period was markedly suppressed by cortical infusion of NMDAR antagonist. The present study reveals that the plasticity and consolidation of orientation selectivity in an early life are dynamically regulated in an experience-dependent manner.     

Development of orientation preference in the mammalian visual cortex.

Recent experiments have studied the development of orientation selectivity in normal animals, visually deprived animals, and animals where patterns of neuronal activity have been altered. Results of these experiments indicate that orientation tuning appears very early in development, and that normal patterns of activity are necessary for its normal development. Visual experience is not needed for early development of orientation, but is crucial for maintaining orientation selectivity. Neuronal activity and vision thus seem to play similar roles in the development of orientation selectivity as they do in the development of eye-specific segregation in the visual system.     

Sensitive period for a multimodal response in human visual motion area MT/MST

The middle temporal complex (MT/MST) is a brain region specialized for the perception of motion in the visual modality. However, this specialization is modified by visual experience: after long-standing blindness, MT/MST responds to sound. Recent evidence also suggests that the auditory response of MT/MST is selective for motion. The developmental time course of this plasticity is not known. To test for a sensitive period in MT/MST development, we used fMRI to compare MT/MST function in congenitally blind, late-blind, and sighted adults. MT/MST responded to sound in congenitally blind adults, but not in late-blind or sighted adults, and not in an individual who lost his vision between ages of 2 and 3 years. All blind adults had reduced functional connectivity between MT/MST and other visual regions. Functional connectivity was increased between MT/MST and lateral prefrontal areas in congenitally blind relative to sighted and late-blind adults. These data suggest that early blindness affects the function of feedback projections from prefrontal cortex to MT/MST. We conclude that there is a sensitive period for visual specialization in MT/MST. During typical development, early visual experience either maintains or creates a vision-dominated response. Once established, this response profile is not altered by long-standing blindness.     

Pooling strategies in V1 can account for the functional and structural diversity across species

Neurons in the primary visual cortex are selective to orientation with various degrees of selectivity to the spatial phase, from high selectivity in simple cells to low selectivity in complex cells. Various computational models have suggested a possible link between the presence of phase invariant cells and the existence of orientation maps in higher mammals’ V1. These models, however, do not explain the emergence of complex cells in animals that do not show orientation maps. In this study, we build a theoretical model based on a convolutional network called Sparse Deep Predictive Coding (SDPC) and show that a single computational mechanism, pooling, allows the SDPC model to account for the emergence in V1 of complex cells with or without that of orientation maps, as observed in distinct species of mammals. In particular, we observed that pooling in the feature space is directly related to the orientation map formation while pooling in the retinotopic space is responsible for the emergence of a complex cells population. Introducing different forms of pooling in a predictive model of early visual processing as implemented in SDPC can therefore be viewed as a theoretical framework that explains the diversity of structural and functional phenomena observed in V1.     

Effect of imbalance in activities between ON- and OFF-center LGN cells on orientation map formation

 It has been reported that the OFF responses of cells in the visual pathway are stronger, on average, than the ON responses early in the life of cats and ferrets. In this study, we theoretically investigate the effects of this imbalance in activity on the orientation map formation. We carry out computer simulations based on our previously proposed self-organization model, in which the correlated activities between ON- and OFF-center cells in the lateral geniculate nucleus regulate the formation of orientation maps in the visual cortex. When imbalance between the activities of these ON- and OFF-center cells is assumed, we obtain orientation maps with spatial periodicity, as observed in the experiments. On the other hand, when balanced activities are assumed, orientation maps do not show periodicity. This suggests that the imbalance in activities between ON- and OFF-center cells contributes to the elaboration of orientation maps during the critical period. Received: 8 July 1999 / Accepted in revised form: 18 February 2000     

Long-range, pattern-dependent contextual effects in early human visual cortex

The standard view of neurons in early visual cortex is that they behave like localized feature detectors. Here we demonstrate that processing in early visual areas goes beyond feature detection by showing that neural responses are greater when a feature deviates from its context compared to when it does not deviate from its context. Using psychophysics, fMRI, and electroencephalography methodologies, we measured neural responses to an oriented Gabor ("target") embedded in various visual patterns as defined by the relative orientation of flanking stimuli. We first show using psychophysical contrast adaptation and fMRI that a target that differs from its context results in more neural activity compared to a target that is contained within an alternating sequence, suggesting that neurons in early visual cortex are sensitive to large-scale orientation patterns. Next, we use event-related potentials to show that orientation deviations affect the earliest sensory components of the target response. Finally, we use forced-choice classification of "noise" stimuli to show that we are more likely to "see" orientations that deviate from the context. Our results suggest that early visual cortex is sensitive to global patterns in images in a way that is markedly different from the predictions of standard models of cortical visual processing.     

On the origin of the functional architecture of the cortex

The basic structure of receptive fields and functional maps in primary visual cortex is established without exposure to normal sensory experience and before the onset of the critical period. How the brain wires these circuits in the early stages of development remains unknown. Possible explanations include activity-dependent mechanisms driven by spontaneous activity in the retina and thalamus, and molecular guidance orchestrating thalamo-cortical connections on a fine spatial scale. Here I propose an alternative hypothesis: the blueprint for receptive fields, feature maps, and their inter-relationships may reside in the layout of the retinal ganglion cell mosaics along with a simple statistical connectivity scheme dictating the wiring between thalamus and cortex. The model is shown to account for a number of experimental findings, including the relationship between retinotopy, orientation maps, spatial frequency maps and cytochrome oxidase patches. The theory's simplicity, explanatory and predictive power makes it a serious candidate for the origin of the functional architecture of primary visual cortex.     

Touch Influences Visual Perception with a Tight Orientation-Tuning

Stimuli from different sensory modalities are thought to be processed initially in distinct unisensory brain areas prior to convergence in multisensory areas. However, signals in one modality can influence the processing of signals from other modalities and recent studies suggest this cross-modal influence may occur early on, even in ‘unisensory’ areas. Some recent psychophysical studies have shown specific cross-modal effects between touch and vision during binocular rivalry, but these cannot completely rule out a response bias. To test for genuine cross-modal integration of haptic and visual signals, we investigated whether congruent haptic input could influence visual contrast sensitivity compared to incongruent haptic input in three psychophysical experiments using a two-interval, two-alternative forced-choice method to eliminate response bias. The initial experiment demonstrated that contrast thresholds for a visual grating were lower when exploring a haptic grating that shared the same orientation compared to an orthogonal orientation. Two subsequent experiments mapped the orientation and spatial frequency tunings for the congruent haptic facilitation of vision, finding a clear orientation tuning effect but not a spatial frequency tuning. In addition to an increased contrast sensitivity for iso-oriented visual-haptic gratings, we found a significant loss of sensitivity for orthogonally oriented visual-haptic gratings. We conclude that the tactile influence on vision is a result of a tactile input to orientation-tuned visual areas.     

Stability of cortical responses and the statistics of natural scenes.

The primary visual cortex (V1) of higher mammals contains maps of stimulus features; how these maps influence vision remains unknown. We have examined the functional significance of an asymmetry in the orientation map in cat V1, i.e., the fact that a larger area of V1 is preferentially activated by vertical and horizontal contours than by contours at oblique orientations. Despite the fact that neurons tuned to cardinal and oblique orientations have indistinguishable tuning characteristics, cardinal neurons remain more stable in their response properties after selective perturbation induced by adaptation. Similarly, human observers report different adaptation-induced changes in orientation tuning between cardinal and oblique axes. We suggest that the larger cortical area devoted to cardinal orientations imposes stability on the processing of cardinal contours during visual perception, by retaining invariant cortical responses along cardinal axes.     

Recording and manipulating the in vivo correlational structure of neuronal activity during visual cortical development.

Many aspects of visual cortical functional architecture, such as orientation and ocular dominance columns, are present before animals have had any visual experience, indicating that the initial formation of cortical circuitry takes place without the influence of environmental cues. For this reason, it has been proposed that spontaneous activity within the developing visual pathway carries instructive information to guide the early establishment of cortical circuits. Recently developed recording and stimulation techniques are revealing new information about the in vivo organization of this spontaneous activity and its contribution to cortical development. Multielectrode recordings in the developing lateral geniculate nucleus (LGN) of ferrets demonstrate that retinal spontaneous activity is not simply relayed to the visual cortex, but is reshaped and transformed by a variety of mechanisms including cortical feedback and endogenous oscillatory activity. The resulting patterns are consistent with many of the predictions of correlation-based models of cortical development. In addition, the introduction of artificially correlated activity into the visual pathway disrupts some but not all aspects of orientation tuning development. Thus, while these results support an instructive role of spontaneous activity in shaping cortical development, there still appears to be a number of aspects of this process that cannot be accounted for by activity alone.     

Ten_m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision

Binocular vision requires an exquisite matching of projections from each eye to form a cohesive representation of the visual world. Eye-specific inputs are anatomically segregated, but in register in the visual thalamus, and overlap within the binocular region of primary visual cortex. Here, we show that the transmembrane protein Ten_m3 regulates the alignment of ipsilateral and contralateral projections. It is expressed in a gradient in the developing visual pathway, which is consistently highest in regions that represent dorsal visual field. Mice that lack Ten_m3 show profound abnormalities in mapping of ipsilateral, but not contralateral, projections, and exhibit pronounced deficits when performing visually mediated behavioural tasks. It is likely that the functional deficits arise from the interocular mismatch, because they are reversed by acute monocular inactivation. We conclude that Ten_m3 plays a key regulatory role in the development of aligned binocular maps, which are required for normal vision.     

Contextual modulation outside of awareness

Contextual effects are ubiquitous in vision and reveal fundamental principles of sensory coding. Here, we demonstrate that an oriented surround grating can affect the perceived orientation of a central test grating even when backward masking of the surround prevents its orientation from being consciously perceived. The effect survives introduction of a gap between test and surround of over a degree even under masking, suggesting either that contextual information can effectively propagate across early visual cortex in the absence of awareness of the signaled context or that it can proceed undetected to higher processing levels at which such horizontal propagation may not be necessary. The effect under masking also shows partial interocular transfer, demonstrating processing of orientation by binocular neurons in visual cortex in the absence of conscious orientation perception. This pattern of results is consistent with the suggestion that simultaneous orientation contrast is mediated at multiple levels of the visual processing hierarchy, and it supports the view that propagation of signals to and, possibly, back from higher visual areas is necessary for conscious perception.     

Magnetic Orientation in the Savannah Sparrow

Although magnetic compass orientation has been reported in a number of invertebrate and vertebrate taxa, including about a dozen migratory bird species, magnetic orientation capabilities in animals remain somewhat controversial. We have hand-raised a large number of Savannah sparrows (Passerculus sandwichensis) to study the ontogeny of orientation behavior. Young birds with a variety of early experience with visual and magnetic orientation cues have been tested for magnetic orientation during their first autumn migration. Here we present data from 80 hand-raised sparrows, each tested several times in both normal and shifted magnetic fields. Birds reared indoors with no experience with visual orientation cues showed axial north-south orientation that shifted by almost exactly the magnitude of 90° clockwise and counterclockwise shifts in the direction of magnetic north. Other groups of birds with varying early experience with visual orientation cues showed different preferred orientation directions, but all groups shifted orientation direction in response to shifts in the magnetic field. The data thus demonstrate a robust magnetic orientation ability in this species.     

Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse

Sensory experience and spontaneous activity play important roles in development of sensory circuits; however, their relative contributions are unclear. Here, we test the role of different forms of activity on remodeling of the mouse retinogeniculate synapse. We found that the bulk of maturation occurs without patterned sensory activity over 4 days spanning eye opening. During this early developmental period, blockade of spontaneous retinal activity by tetrodotoxin, but not visual deprivation, retarded synaptic strengthening and inhibited pruning of excess retinal afferents. Later in development, synaptic remodeling becomes sensitive to changes in visually evoked activity, but only if there has been previous visual experience. Synaptic strengthening and pruning were disrupted by visual deprivation following 1 week of vision, but not by chronic deprivation from birth. Thus, spontaneous activity is necessary to drive the bulk of synaptic refinement around the time of eye opening, while sensory experience is important for the subsequent maintenance of connections.     

Subjective figures and texture perception

A texture discrimination task using the Ehrenstein illusion demonstrates that subjective brightness effects can play an essential role in early vision. The subjectively bright regions of the Ehrenstein can be organized either as discs or as stripes, depending on orientation. The accuracy of discrimination between variants of the Ehrenstein and control patterns was a direct function of the presence of the illusory brightness stripes, being high when they were present and low otherwise. It is argued that neither receptive field structure nor spatial-frequency content can adequately account for these results. We suggest that the subjective brightness illusions, rather than being a high-level, cognitive aspect of vision, are in fact the result of an early visual process.     

Ten_m3 Regulates Eye-Specific Patterning in the Mammalian Visual Pathway and Is Required for Binocular Vision

Binocular vision requires an exquisite matching of projections from each eye to form a cohesive representation of the visual world. Eye-specific inputs are anatomically segregated, but in register in the visual thalamus, and overlap within the binocular region of primary visual cortex. Here, we show that the transmembrane protein Ten_m3 regulates the alignment of ipsilateral and contralateral projections. It is expressed in a gradient in the developing visual pathway, which is consistently highest in regions that represent dorsal visual field. Mice that lack Ten_m3 show profound abnormalities in mapping of ipsilateral, but not contralateral, projections, and exhibit pronounced deficits when performing visually mediated behavioural tasks. It is likely that the functional deficits arise from the interocular mismatch, because they are reversed by acute monocular inactivation. We conclude that Ten_m3 plays a key regulatory role in the development of aligned binocular maps, which are required for normal vision.     

Development of orientation selectivity in the primary visual cortex of normally and dark reared kittens

The development of orientation selectivity in the primary visual cortex is described by first-order kinetics between three functional compartments chained in a catenary mode. A first model is presented, in which two unidirectional kinetics with constant exchange coefficients, symmetrical in their effects, function in an alternating mode depending on the presence or absence of visual experience. The failure of this model to simulate the modifications induced by a delayed visual experience, when the exchange coefficients are identified to fit normal and dark rearing, supports the hypothesis that the maturation process consequent to interaction with visual environment is dependent on the date at which it is allowed to take place. A second model is then proposed, in which exchange coefficients are piecewise linear functions of time. In order to correctly predict the functional effects of restricted visual experience following prior dark rearing, it is assumed that visuomotor experience during the critical period permits the expression of a non-linear modifiability gradient which may have been masked up to this point by the absence of vision or eye movements.     

Transient attention enhances perceptual performance and FMRI response in human visual cortex

When a visual stimulus suddenly appears, it captures attention, producing a transient improvement of performance on basic visual tasks. We investigate the effect of transient attention on stimulus representations in early visual areas using rapid event-related fMRI. Participants discriminated the orientation of one of two gratings preceded or followed by a nonpredictive peripheral cue. Compared to control conditions, precueing the target location improved performance and produced a larger fMRI response in corresponding retinotopic areas. This enhancement progressively increased from striate to extrastriate areas. Control conditions indicated that the enhanced fMRI response was not due to sensory summation of cue and target signals. Thus, an uninformative precue increases both perceptual performance and the concomitant stimulus-evoked activity in early visual areas. These results provide evidence regarding the retinotopically specific neural correlate for the effects of transient attention on early vision.     

Experience in early infancy is indispensable for color perception

Early visual experience is indispensable to shape the maturation of cortical circuits during development. Monocular deprivation in infancy, for instance, leads to an irreversible reduction of visually driven activity in the visual cortex through the deprived eye and a loss of binocular depth perception. It was tested whether or not early experience is also necessary for color perception. Infant monkeys were reared for nearly a year in a separate room where the illumination came from only monochromatic lights. After extensive training, they were able to perform color matching. But, their judgment of color similarity was quite different from that of normal animals. Furthermore, they had severe deficits in color constancy; their color vision was very much wavelength dominated, so they could not compensate for the changes in wavelength composition. These results indicate that early visual experience is also indispensable for normal color perception.