Onset Of Visual Experience Research Articles

Spontaneous Retinal Waves Can Generate Long-Range Horizontal Connectivity in Visual Cortex.

In the primary visual cortex (V1) of higher mammals, long-range horizontal connections (LHCs) are observed to develop, linking iso-orientation domains of cortical tuning. It is unknown how this feature-specific wiring of circuitry develops before eye-opening. Here, we suggest that LHCs in V1 may originate from spatiotemporally structured feedforward activities generated from spontaneous retinal waves. Using model simulations based on the anatomy and observed activity patterns of the retina, we show that waves propagating in retinal mosaics can initialize the wiring of LHCs by coactivating neurons of similar tuning, whereas equivalent random activities cannot induce such organizations. Simulations showed that emerged LHCs can produce the patterned activities observed in V1, matching the topography of the underlying orientation map. The model can also reproduce feature-specific microcircuits in the salt-and-pepper organizations found in rodents. Our results imply that early peripheral activities contribute significantly to cortical development of functional circuits.SIGNIFICANCE STATEMENT Long-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, thereby selectively connecting iso-domains of orientation map. However, it is unknown how such feature-specific wirings develop before eye-opening. Here, we show that LHCs in V1 may originate from the feature-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings in the V1 neurons. Our model also explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is universally applicable to circuits of various mammalian species.

Development of Cross-Orientation Suppression and Size Tuning and the Role of Experience.

Many sensory neural circuits exhibit response normalization, which occurs when the response of a neuron to a combination of multiple stimuli is less than the sum of the responses to the individual stimuli presented alone. In the visual cortex, normalization takes the forms of cross-orientation suppression and surround suppression. At the onset of visual experience, visual circuits are partially developed and exhibit some mature features such as orientation selectivity, but it is unknown whether cross-orientation suppression is present at the onset of visual experience or requires visual experience for its emergence. We characterized the development of normalization and its dependence on visual experience in female ferrets. Visual experience was varied across the following three conditions: typical rearing, dark rearing, and dark rearing with daily exposure to simple sinusoidal gratings (14-16 h total). Cross-orientation suppression and surround suppression were noted in the earliest observations, and did not vary considerably with experience. We also observed evidence of continued maturation of receptive field properties in the second month of visual experience: substantial length summation was observed only in the oldest animals (postnatal day 90); evoked firing rates were greatly increased in older animals; and direction selectivity required experience, but declined slightly in older animals. These results constrain the space of possible circuit implementations of these features.SIGNIFICANCE STATEMENT The development of the brain depends on both nature-factors that are independent of the experience of an individual animal-and nurture-factors that depend on experience. While orientation selectivity, one of the major response properties of neurons in visual cortex, is already present at the onset of visual experience, it is unknown whether response properties that depend on interactions among multiple stimuli develop without experience. We find that the properties of cross-orientation suppression and surround suppression are present at eye opening, and do not depend on visual experience. Our results are consistent with the idea that a majority of the basic properties of sensory neurons in primary visual cortex are derived independent of the experience of an individual animal.

A hierarchical, retinotopic proto-organization of the primate visual system at birth.

The adult primate visual system comprises a series of hierarchically organized areas. Each cortical area contains a topographic map of visual space, with different areas extracting different kinds of information from the retinal input. Here we asked to what extent the newborn visual system resembles the adult organization. We find that hierarchical, topographic organization is present at birth and therefore constitutes a proto-organization for the entire primate visual system. Even within inferior temporal cortex, this proto-organization was already present, prior to the emergence of category selectivity (e.g., faces or scenes). We propose that this topographic organization provides the scaffolding for the subsequent development of visual cortex that commences at the onset of visual experience.

Postnatal Dendritic Growth and Spinogenesis of Layer-V Pyramidal Cells Differ between Visual, Inferotemporal, and Prefrontal Cortex of the Macaque Monkey.

Pyramidal cells in the primate cerebral cortex, particularly those in layer III, exhibit regional variation in both the time course and magnitude of postnatal growth and pruning of dendrites and spines. Less is known about the development of pyramidal cell dendrites and spines in other cortical layers. Here we studied dendritic morphology of layer-V pyramidal cells in primary visual cortex (V1, sensory), cytoarchitectonic area TE in the inferotemporal cortex (sensory association), and granular prefrontal cortex (Walker's area 12, executive) of macaque monkeys at the ages of 2 days, 3 weeks, 3.5 months, and 4.5 years. We found that changes in the basal dendritic field area of pyramidal cells were different across the three areas. In V1, field size became smaller over time (largest at 2 days, half that size at 4.5 years), in TE it did not change, and in area 12 it became larger over time (smallest at 2 days, 1.5 times greater at 4.5 years). In V1 and TE, the total number of branch points in the basal dendritic trees was similar between 2 days and 4.5 years, while in area 12 the number was greater in the adult monkeys than in the younger ones. Spine density peaked at 3 weeks and declined in all areas by adulthood, with V1 exhibiting a faster decline than area TE or area 12. Estimates of the total number of spines in the dendritic trees revealed that following the onset of visual experience, pyramidal cells in V1 lose more spines than they grow, whereas those in TE and area 12 grow more spines than they lose during the same period. These data provide further evidence that the process of synaptic refinement in cortical pyramidal cells differs not only according to time, but also location within the cortex. Furthermore, given the previous finding that layer-III pyramidal cells in all these areas exhibit the highest density and total number of spines at 3.5 months, the current results indicate that pyramidal cells in layers III and V develop spines at different rates.

Visual Stimulus Speed Does Not Influence the Rapid Emergence of Direction Selectivity in Ferret Visual Cortex

Sensory experience is necessary for the development of some receptive field properties of neurons in primary sensory cortical areas. However, it remains unclear whether the parameters of an individual animal's experience play an instructive role and influence the tuning parameters of cortical sensory neurons as selectivity emerges, or rather whether experience merely permits the completion of processes that are fully seeded at the onset of experience. Here we have examined whether the speed of visual stimuli that are presented to visually naive ferrets can influence the parameters of speed tuning and direction selectivity in cortical neurons. Visual experience is necessary for the development of direction selectivity in carnivores. If, during development, cortical neurons had the flexibility to choose from among different inputs with a range of spatial positions and temporal delays, then correlation-based plasticity mechanisms could instruct the precise spatiotemporal selectivity that underlies speed tuning and direction selectivity, and the parameters of an individual animal's experience would influence the tuning that emerges. Alternatively, the tuning parameters of these neurons may already be established at the onset of visual experience, and experience may merely permit the expression of this tuning. We found that providing different groups of animals with either slow (12.5 deg/s) or fast (50 deg/s) visual stimuli resulted in emergence of direction selectivity, but that speed tuning and direction selectivity were similar in the two groups. These results are more consistent with a permissive role for experience in the development of direction selectivity.SIGNIFICANCE STATEMENT The proper development of brain circuits and neural response properties depends on both nature (factors independent of experience) and nurture (factors dependent on experience). In this study, we examined whether the quality of visual experience of an individual animal influences the development of basic sensory detectors in primary visual cortex. We found that, although visual experience is required for the development of direction selectivity, tuning for stimulus speed could not be altered by specific experience with slow or fast stimuli. These results suggest that the tuning parameters for direction selectivity are specified independently of an animal's sensory experience, and that a range of experiences can promote the proper mature expression of direction selectivity in primary visual cortex.

Infants’ statistical learning: 2- and 5-month-olds’ segmentation of continuous visual sequences

Past research suggests that infants have powerful statistical learning abilities; however, studies of infants’ visual statistical learning offer differing accounts of the developmental trajectory of and constraints on this learning. To elucidate this issue, the current study tested the hypothesis that young infants’ segmentation of visual sequences depends on redundant statistical cues to segmentation. A sample of 20 2-month-olds and 20 5-month-olds observed a continuous sequence of looming shapes in which unit boundaries were defined by both transitional probability and co-occurrence frequency. Following habituation, only 5-month-olds showed evidence of statistically segmenting the sequence, looking longer to a statistically improbable shape pair than to a probable pair. These results reaffirm the power of statistical learning in infants as young as 5months but also suggest considerable development of statistical segmentation ability between 2 and 5months of age. Moreover, the results do not support the idea that infants’ ability to segment visual sequences based on transitional probabilities and/or co-occurrence frequencies is functional at the onset of visual experience, as has been suggested previously. Rather, this type of statistical segmentation appears to be constrained by the developmental state of the learner. Factors contributing to the development of statistical segmentation ability during early infancy, including memory and attention, are discussed.

Emergence of feature-specific connectivity in cortical microcircuits in the absence of visual experience.

In primary visual cortex (V1), connectivity between layer 2/3 (L2/3) excitatory neurons undergoes extensive reorganization after the onset of visual experience whereby neurons with similar feature selectivity form functional microcircuits (Ko et al., 2011, 2013). It remains unknown whether visual experience is required for the developmental refinement of intracortical circuitry or whether this maturation is guided intrinsically. Here, we correlated the connectivity between V1 L2/3 neurons assayed by simultaneous whole-cell recordings in vitro to their response properties measured by two-photon calcium imaging in vivo in dark-reared mice. We found that neurons with similar responses to oriented gratings or natural movies became preferentially connected in the absence of visual experience. However, the relationship between connectivity and similarity of visual responses to natural movies was not as strong in dark-reared as in normally reared mice. Moreover, dark rearing prevented the normally occurring loss of connections between visually nonresponsive neurons after eye opening (Ko et al., 2013). Therefore, our data suggest that the absence of visual input does not prevent the emergence of functionally specific recurrent connectivity in cortical circuits; however, visual experience is required for complete microcircuit maturation.

Following the ontogeny of retinal waves: pan‐retinal recordings of population dynamics in the neonatal mouse

The immature retina generates spontaneous waves of spiking activity that sweep across the ganglion cell layer during a limited period of development before the onset of visual experience. The spatiotemporal patterns encoded in the waves are believed to be instructive for the wiring of functional connections throughout the visual system. However, the ontogeny of retinal waves is still poorly documented as a result of the relatively low resolution of conventional recording techniques. Here, we characterize the spatiotemporal features of mouse retinal waves from birth until eye opening in unprecedented detail using a large-scale, dense, 4096-channel multielectrode array that allowed us to record from the entire neonatal retina at near cellular resolution. We found that early cholinergic waves propagate with random trajectories over large areas with low ganglion cell recruitment. They become slower, smaller and denser when GABAA signalling matures, as occurs beyond postnatal day (P) 7. Glutamatergic influences dominate from P10, coinciding with profound changes in activity dynamics. At this time, waves cease to be random and begin to show repetitive trajectories confined to a few localized hotspots. These hotspots gradually tile the retina with time, and disappear after eye opening. Our observations demonstrate that retinal waves undergo major spatiotemporal changes during ontogeny. Our results support the hypotheses that cholinergic waves guide the refinement of retinal targets and that glutamatergic waves may also support the wiring of retinal receptive fields.

Development of visual perception.

Processes of visual development that yield a view of the world as coherent and stable begin well before birth and extend over the first several years after the onset of visual experience. Infants are born capable of seeing and with specific preferences that guide the point of gaze to relevant portions of the visual scene to support learning about objects and faces. Visual development after birth is characterized by critical periods in many notable visual functions, and by extensive learning from experience and increasing control over eye movement systems. WIREs Cogni Sci 2011 2 515-528 DOI: 10.1002/wcs.128 For further resources related to this article, please visit the WIREs website.

Spinogenesis and Pruning from Early Visual Onset to Adulthood: An Intracellular Injection Study of Layer III Pyramidal Cells in the Ventral Visual Cortical Pathway of the Macaque Monkey

Neocortical pyramidal cells are characterized by markedly different structure among cortical areas in the mature brain. In the ventral visual pathway of adult primates, pyramidal cells become increasingly more branched and more spinous with anterior progression through the primary (V1), second (V2), and fourth (V4) visual areas and cytoarchitectonic areas TEO and TE. It is not known how these regional specializations in neuron structure develop. Here, we report that the basal dendritic trees of layer III pyramidal cells in V1, V2, V4, TEO, and TE were characterized by unique growth profiles. Different numbers of spines were grown in the dendritic trees of cells among these cortical areas and then subsequently pruned. In V1, V2, and V4, more spines were pruned than grew resulting in a net decrease in the number of spines in the dendritic trees following the onset of visual experience. In TEO and TE, neurons grew more spines than they pruned from visual onset to adulthood. These data suggest that visual experience may influence neuronal maturation in different ways in different cortical areas.

Spinogenesis and Pruning Scales across Functional Hierarchies

Spinogenesis and synaptic pruning during development are widely believed to subserve connectional specificity in the mature CNS via Hebbian-type reinforcement. Refinement of neuronal circuit through this "use it or lose it" principle is considered critical for brain development. Here we demonstrate that the magnitude of spinogenesis and pruning in the basal dendritic trees of pyramidal cells differ dramatically among sensory, association, and executive cortex. Moreover, somewhat counterintuitively, we demonstrate that the dendritic trees of pyramidal cells in the primary visual area actually lose more spines than they grow following the onset of visual experience. The present findings reveal that the process of synaptic refinement differs not only according to time, but also location.

Infants' perception of object trajectories.

Filling in the gaps in what humans see is a fundamental perceptual skill, but little is known about the developmental origins of occlusion perception. Three experiments were conducted with infants between 2 and 6 months of age to investigate perception of the continuity of an object trajectory that was briefly occluded. The pattern of results across experiments provided little evidence of veridical responses to trajectory occlusion in the youngest infants, but by 6 months, perceptual completion was more robust. Four-month-olds' responses indicated that they perceived continuity under a short duration of occlusion, but when the object was out of sight for a longer interval, they appeared to perceive the trajectory as discontinuous. These results suggest that perceptual completion of a simple object trajectory (and, by logical necessity, veridical object perception) is not functional at birth but emerges across the first several months after onset of visual experience.

The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex.

Sensory experience begins when neural circuits in the cerebral cortex are still immature; however, the contribution of experience to cortical maturation remains unclear. In the visual cortex, the selectivity of neurons for oriented stimuli at the time of eye opening is poor and increases dramatically after the onset of visual experience. Here we investigate whether visual experience has a significant role in the maturation of orientation selectivity and underlying cortical circuits using two forms of deprivation: dark rearing, which completely eliminates experience, and binocular lid suture, which alters the pattern of sensory driven activity. Orientation maps were present in dark-reared ferrets, but fully mature levels of tuning were never attained. In contrast, only rudimentary levels of orientation selectivity were observed in lid-sutured ferrets. Despite these differences, horizontal connections in both groups were less extensive and less clustered than normal, suggesting that long-range cortical processing is not essential for the expression of orientation selectivity, but may be needed for the full maturation of tuning. Thus, experience is beneficial or highly detrimental to cortical maturation, depending on the pattern of sensory driven activity.

Competition in retinogeniculate patterning driven by spontaneous activity.

When contacts are first forming in the developing nervous system, many neurons generate spontaneous activity that has been hypothesized to shape appropriately patterned connections. In Mustela putorius furo, monocular intraocular blockade of spontaneous retinal waves of action potentials by cholinergic agents altered the subsequent eye-specific lamination pattern of the lateral geniculate nucleus (LGN). The projection from the active retina was greatly expanded into territory normally belonging to the other eye, and the projection from the inactive retina was substantially reduced. Thus, interocular competition driven by endogenous retinal activity determines the pattern of eye-specific connections from retina to LGN, demonstrating that spontaneous activity can produce highly stereotyped patterns of connections before the onset of visual experience.