Does experience provide a permissive or instructive influence on the development of direction selectivity in visual cortex?

In principle, the development of sensory receptive fields in cortex could arise from experience-independent mechanisms that have been acquired through evolution, or through an online analysis of the sensory experience of the individual animal. Here we review recent experiments that suggest that the development of direction selectivity in carnivore visual cortex requires experience, but also suggest that the experience of an individual animal cannot greatly influence the parameters of the direction tuning that emerges, including direction angle preference and speed tuning. The direction angle preference that a neuron will acquire can be predicted from small initial biases that are present in the naïve cortex prior to the onset of visual experience. Further, experience with stimuli that move at slow or fast speeds does not alter the speed tuning properties of direction-selective neurons, suggesting that speed tuning preferences are built in. Finally, unpatterned optogenetic activation of the cortex over a period of a few hours is sufficient to produce the rapid emergence of direction selectivity in the naïve ferret cortex, suggesting that information about the direction angle preference that cells will acquire must already be present in the cortical circuit prior to experience. These results are consistent with the idea that experience has a permissive influence on the development of direction selectivity.     

Responses of squirrel visual cortex neurons to patterned visual stimuli]

The responses of visual cortical neurons to patterned visual stimuli were studied in squirrel Sciurus vulgaris. The direction selective, orientation-selective and non-selective neurons were observed. Most direction-selective and non-selective neurons were sensitive to high speeds of stimulus movement--hundreds deg/s. The direction-selective neurons exhibited their selectivity at such high speeds in spite of the short time of the stimulus movement through the receptive field. Orientation-selective neurons (with simple or complex receptive fields) were sensitive to lower speeds of the stimulus movement (tens deg/s). Some mechanisms of the properties described are discussed.     

Direction-specific adaptation in area MT of the owl monkey

Single neurons were recorded in owl monkey middle temporal visual cortex (MT). Directional neurons showed direction-selective adaptation to pattern motion: responses to motion in the preferred direction were reduced by adaptation to motion in the preferred direction and enhanced by adaptation in the opposite direction. Non-directional neurons did not show significant adaptation.     

Histogenesis of ferret somatosensory cortex

The ferret has emerged as an important animal model for the study of neocortical development. Although detailed studies of the birthdates of neurons populating the ferret visual cortex are available, the birthdates of neurons that reside in somatosensory cortex have not been determined. The current study used bromodeoxyuridine to establish when neurons inhabiting the somatosensory cortex are generated in the ferret; some animals also received injections of [³H]thymidine. In contrast to reports of neurogenesis in ferret visual cortex, most neurons populating the somatosensory cortex have been generated by birth. Although components of all somatosensory cortical layers have been produced at postnatal day 0, the layers are not distinctly formed but develop over a period of several weeks. A small number of neurons continue to be produced for a few days postnatally. The majority of cells belonging to a given layer are born over a period of approximately 3 days, although the subplate and last (layer 2) generated layer take somewhat longer. Although neurogenesis of the neocortex begins along a similar time line for visual and somatosensory cortex, the neurons populating the visual cortex lag substantially during the generation of layer 4, which takes more than 1 week for ferret visual cortex. Layer formation in ferret somatosensory cortex follows many established principles of cortical neurogenesis, such as the well-known inside-out development of cortical layers and the rostro-to-caudal progression of cell birth. In comparison with the development of ferret visual cortex, however, the generation of the somatosensory cortex occurs remarkably early and may reflect distinct differences in mechanisms of development between the two sensory areas. J. Comp. Neurol. 387:179–193, 1997. © 1997 Wiley-Liss, Inc.     

Detector neurons of the visual cortex of the chipmunk

Three functional classes of neurons are described in the Siberian chipmunk visual cortex: neurons nonselective to movement direction, movement-direction-selective neurons and orientation-selective neurons. Nonselective and direction-selective neurons showed maximum adaptiveness at high speeds of movement: 100-500 degrees/s and more. Most of orientation-selective neurons were maximally activated at speeds 10-50 degrees/s. For all neuronal classes a clear-cut correlation between selectivity and movement speed as well as pattern of responses to stationary stimuli in the receptive field were found. The data obtained allowed a division of the neurons into two groups: phasically-fast and tonically-slow with predominance of the first group.     

Direction-selective motion blindness after unilateral posterior brain damage

Motion blindness (MB) is defined as the selective disturbance of visual motion perception despite intact perception of other features of the visual scene. MB is characterized by a pandirectional deficit of motion direction discrimination and is assumed to result from damage to the visual motion pathway, especially area MT/V5. However, the most characteristic feature of primate MT/V5 neurons is not their motion selectivity but their preference for one direction of motion (direction selectivity), which changes incrementally at neighbouring columns. In addition to this microscopic directional organization, studies in nonhuman and human primates suggest that single directions of motion are also coded at a more macroscopic level. We thus hypothesized that if MB in humans results from damage to direction-selective neurons in the visual motion pathway, posterior brain damage might cause MB which is direction selective, not pandirectional. The present study investigated motion direction discrimination in patients with posterior unilateral brain damage and determined separate psychophysical thresholds for the four cardinal directions. In addition, we analysed whether the direction of erroneous motion perception (i.e. the perception of right motion for upward motion) was random or showed a directional bias. We report three principal findings. First, motion direction discrimination was severely impaired in one or two directions while it was normal in the other directions. This constituted direction-selective MB. Second, MB was characterized not only by a quantitative direction-selective increase in psychophysical thresholds but also by a qualitative impairment of perceiving motion direction systematically in wrong directions. Both findings suggest that the cortical modules specialized for the perception of a single direction of motion might be larger than previously thought. Third, lesion analysis showed that unilateral damage, not only the human homologue of MT/V5 but also to parieto-occipital cortex, leads to MB.     

Dynamics of population response to changes of motion direction in primary visual cortex

The visual system is thought to represent the direction of moving objects in the relative activity of large populations of cortical neurons that are broadly tuned to the direction of stimulus motion, but how changes in the direction of a moving stimulus are represented in the population response remains poorly understood. Here we take advantage of the orderly mapping of direction selectivity in ferret primary visual cortex (V1) to explore how abrupt changes in the direction of a moving stimulus are encoded in population activity using voltage-sensitive dye imaging. For stimuli moving in a constant direction, the peak of the V1 population response accurately represented the direction of stimulus motion, but following abrupt changes in motion direction, the peak transiently departed from the direction of stimulus motion in a fashion that varied with the direction offset angle and was well predicted from the response to the component directions. We conclude that cortical dynamics and population coding mechanisms combine to place constraints on the accuracy with which abrupt changes in direction of motion can be represented by cortical circuits.     

Visual direction-selective neurons in the pretectum of the rainbow trout

In mammals, the essential neuronal substrate for the generation of the horizontal optokinetic nystagmus (hOKN) are the nucleus of optical tract (NOT) and the dorsal terminal nucleus (DTN). The medial terminal nucleus (MTN) is thought to be involved in vertical OKN control. Characteristic for all of these neurons is a high-direction selectivity. Although behavioural hOKN experiments in different fish species show comparability to mammals, little is known about the neuronal OKN control in fish. In preceding studies, we demonstrated that the rainbow trout has a nearly symmetrical monocular hOKN at low stimulus speeds. With increasing visual stimulus speeds (>14 degrees /s), the monocular hOKN becomes asymmetrical with a temporo to nasal preferred direction. For visual stimulation, we presented random-dot-patterns projected by a planetarium inside a perimeter. We tested four rotation axes of the planetarium, yaw (0 degrees -180 degrees ), roll (90 degrees -270 degrees ), diagonal (45 degrees -225 degrees ) and anti-diagonal (135 degrees -315 degrees ). In every position, the visual stimulus turned in clockwise and counter-clockwise direction. In a subregion of the pretectum of nine fish, we recorded 47 direction-selective neurons. Analysis of tuning-curves and preferred direction vectors show that these neurons encode both horizontal (yaw) and vertical (roll) visual stimulus directions. These results suggest that the control of horizontal and vertical OKN might not segregate into different nuclei in fish.     

Development of cortical influences on superior colliculus multisensory neurons: effects of dark‐rearing

Rearing cats from birth to adulthood in darkness prevents neurons in the superior colliculus (SC) from developing the capability to integrate visual and non‐visual (e.g. visual‐auditory) inputs. Presumably, this developmental anomaly is due to a lack of experience with the combination of those cues, which is essential to form associative links between them. The visual‐auditory multisensory integration capacity of SC neurons has also been shown to depend on the functional integrity of converging visual and auditory inputs from the ipsilateral association cortex. Disrupting these cortico‐collicular projections at any stage of life results in a pattern of outcomes similar to those found after dark‐rearing; SC neurons respond to stimuli in both sensory modalities, but cannot integrate the information they provide. Thus, it is possible that dark‐rearing compromises the development of these descending tecto‐petal connections and the essential influences they convey. However, the results of the present experiments, using cortical deactivation to assess the presence of cortico‐collicular influences, demonstrate that dark‐rearing does not prevent the association cortex from developing robust influences over SC multisensory responses. In fact, dark‐rearing may increase their potency over that observed in normally‐reared animals. Nevertheless, their influences are still insufficient to support SC multisensory integration. It appears that cross‐modal experience shapes the cortical influence to selectively enhance responses to cross‐modal stimulus combinations that are likely to be derived from the same event. In the absence of this experience, the cortex develops an indiscriminate excitatory influence over its multisensory SC target neurons.     

Responses of neurons in the Clare-Bishop cortical association area of the cat cerebral cortex to photic stimulation

In acute experiments on cats with protrigeminal section immobilized by flaxedil the electrical activity of single neurons in associative visual cortex of Clare-Bishop was investigated by the extracellular registration of their spike activity. 95.5% of investigated neurons responding to natural stimulation (light spots) were sensitive to the movement of stimulus through the receptive field. Nearly 55% of neurons exhibited selective responses to the direction of stimulus movement. Some neurones responded only when the stimulus was crossing the border points of receptive field. Nearly 85.3% of neurons responded to the flashing spot with "on", "on-off" and "off" reactions, and also to the stimulation by diffuse flashes. Receptive fields of neurons in the Clare-Bishop area were of strip-like form with longitudinal axis in horizontal orientation. Presented observations allow concluding that the Clare-Bishop cortical association area plays an essential role in the central processing of visual information.     

Inhibitory components in responses of neurons of the lateral suprasylvian area of the cat cortex

Inhibitory components of neuronal responses to moving visual stimuli in the lateral suprasylvian area of the cat cortex have been studied. Comparison of PST histograms of responses to two opposite directions of the movement allows revealing changes in the spatial localization of discharge centres in receptive fields relative to the movement direction. In all neurons investigated which revealed monotonous stationary structure of receptive fields no subregions coincidental with the inhibitory components of the responses are found. The presented experiments have promoted a conclusion that inhibitory components of responses of observed neurons could represent aftereffects following excitation of the cell when the stimulus is crossing the discharge centre of the receptive field.     

Investigating visual motion perception using the transcranial magnetic stimulation-adaptation paradigm

The state-dependency approach of transcranial magnetic stimulation (TMS) enables differential stimulation of functionally distinct neural populations within the affected region of cortex. Here we tested the validity of a paradigm based on state-dependency, the TMS-adaptation paradigm, in the context of visual motion perception. Visual adaptation was used to induce an activity imbalance in direction-selective neurons in the visual cortex, after which participants performed a motion direction discrimination task. When TMS was applied over the motion-selective area V5/MT before each experimental trial, the detection of the direction encoded by the adapted neurons was facilitated relative to the direction encoded by the nonadapted neurons. This finding demonstrates, in the domain of visual motion detection, the state-dependency of TMS effects and the validity of the TMS-adaptation paradigm.     

Mechanisms for binocular depth sensitivity along the vertical meridian of the visual field

By removing the visual cortex unilaterally, and recording along the intact 17/18 border, we have investigated the influence of the corpus callosum on the tuning curves for stimulus disparity of cat cortical neurons. Responses to binocular stimulation were examined to movement in the same (in-phase) and in the opposite direction (antiphase) across the two retinae. In lesioned cats, as in normal cats, units were encountered which showed high sensitivity and narrow tuning for stimulus disparity. In contrast to normal cats, however, lesioned cats showed a reduced proportion of units displaying moderate binocular interactions, as well as a substantial increase in disparity-insensitive cells. The loss of disparity sensitivity after decortication was associated with a reduced incidence of both selectivity for the direction of stimulus motion and binocular activation. No large differences between the preparations were seen, however, in the ocular dominance of the total populations of cells. Differences between the normal and lesioned cats were found in binocular responses to in-phase but not to antiphase stimulation motion. Tuning curves in lesioned cats showed reduced binocular inhibition but no changes in binocular facilitation. Our findings indicate that callosal input contributes to unit disparity sensitivity by enhancing direction-selective binocular inhibition. The corpus callosum generates disparity sensitivity in a population of units in the superficial cortical layers which may play a particular role in the perception of stereoscopic depth.     

Direction selectivity of excitatory and inhibitory neurons in ferret visual cortex.

Direction selectivity is a characteristic feature of neurons in the visual cortex of higher mammals. Excitatory and inhibitory cortical neurons receive different patterns of synaptic connections resulting in different receptive field properties. We have analyzed the direction tuning of excitatory and inhibitory neurons of ferret visual cortex using single unit recordings. Direction tuning was constant among neurons in a vertical column. The majority (> 80%) of excitatory (regular spiking) neurons were direction tuned or direction biased. Fast spiking (inhibitory) neurons were orientation, but only weakly or not direction tuned. This indicates that excitatory and inhibitory neurons have different functions in visual processing and their different integration in thalamocortical and intracortical circuits results in a diversification of receptive field properties.     

Figure-Ground Segregation at Contours: a Neural Mechanism in the Visual Cortex of the Alert Monkey

An important task of vision is the segregation of figure and ground in situations of spatial occlusion. Psychophysical evidence suggests that the depth order at contours is defined early in visual processing. We have analysed this process in the visual cortex of the alert monkey. The animals were trained on a visual fixation task which reinforced foveal viewing. During periods of active visual fixation, we recorded the responses of single neurons in striate and prestriate cortex (areas V1, V2, and V3/V3A). The stimuli mimicked situations of spatial occlusion, usually a uniform light (or dark) rectangle overlaying a grating texture of opposite contrast. The direction of figure and ground at the borders of these rectangles was defined by the direction of the terminating grating lines (occlusion cues). Neuronal responses were analysed with respect to figure-ground direction and contrast polarity at such contours. Striate neurons often failed to respond to such stimuli, or were selective for contrast polarity; others were non-selective. Some neurons preferred a certain combination of figure-ground direction and contrast polarity. These neurons were rare both in striate and prestriate cortex. The majority of neurons signalled figure-ground direction independent of contrast polarity. These neurons were only found in prestriate cortex. We explain these responses in terms of a model which also explains neuronal signals of illusory contours. These results suggest that occlusion cues are used at an early level of processing to segregate figure and ground at contours.     

Development of monotonic neuronal tuning in the monkey inferotemporal cortex through long-term learning of fine shape discrimination

Visual expertise in discriminating fine differences among a group of similar objects can be obtained through extensive long-term training. Here we investigated the neural bases of this superior capability. The inferotemporal cortex, located at the final stage along the ventral visual pathway, was a candidate site in monkeys because cells there respond to various complex features of objects. To identify the changes that underlie the development of visual expertise in fine discrimination, we created a set of parametrically designed object stimuli and compared the stimulus selectivity of inferotemporal cells between two different training histories. One group of recordings was conducted after the monkeys had been extensively trained for fine discrimination (fine-discrimination period) and the other after the monkeys had been exposed only for coarse discrimination (coarse-discrimination period). We found that the tuning of responses recorded in the fine-discrimination period was more monotonic in the stimulus parameter space. The stimuli located at the extreme in the parameter space evoked the maximum responses in a larger proportion of cells and the direction of response decrease in the parameter space was more consistent. Moreover, the stimulus arrangement reconstructed from the responses recorded during the fine-discrimination period was more similar to the original stimulus arrangement. These results suggest that visual expertise could be based on the development, in the inferotemporal cortex, of neuronal selectivity monotonically tuned over the parameter space of the object images.     

Dynamics of macaque MT cell responses to grating triplets

Neurons in area MT are sensitive to the direction of motion of gratings and of plaids made by summing 2 gratings moving in different directions. MT component direction-selective (CDS) neurons respond to the individual gratings of a plaid. Pattern direction-selective (PDS) neurons on the other hand, combine component information and respond selectively to the resulting pattern motion. Adding a third grating creates a "triplaid," which contains 3 grating and 3 plaid motions and is perceptually multistable. To examine how direction-selective mechanisms parse the motion signals in triplaids, we recorded MT responses of anesthetized and awake macaques to stimuli in which 3 identical moving gratings whose directions were separated by 120° were introduced in 3 successive epochs, going from grating to plaid to triplaid. CDS and PDS neurons-selected based on their responses to gratings and plaids-had strikingly different tuning properties in the triplaid epoch. CDS neurons were strongly tuned for the direction of motion of individual gratings, but PDS neurons nearly lost their selectivity for either the gratings or the plaids in the stimulus. We explain this reduced motion selectivity with a model that relates pattern selectivity of PDS neurons to a broad pooling of V1 afferents with a near-cosine weighting profile. Because PDS neurons signal both component and pattern motion in gratings and plaids, their reduced selectivity for motion in triplaids may be what makes these stimuli perceptually multistable.     

Visual Familiarity Induced 5-Hz Oscillations and Improved Orientation and Direction Selectivities in V1

Neural oscillations play critical roles in information processing, communication between brain areas, learning, and memory. We have recently discovered that familiar visual stimuli can robustly induce 5-Hz oscillations in the primary visual cortex (V1) of awake mice after the visual experience. To gain more mechanistic insight into this phenomenon, we used in vivo patch-clamp recordings to monitor the subthreshold activity of individual neurons during these oscillations. We analyzed the visual tuning properties of V1 neurons in naive and experienced mice to assess the effect of visual experience on the orientation and direction selectivity. Using optogenetic stimulation through the patch pipette in vivo, we measured the synaptic strength of specific intracortical and thalamocortical projections in vivo in the visual cortex before and after the visual experience. We found 5-Hz oscillations in membrane potential (V_m) and firing rates evoked in single neurons in response to the familiar stimulus, consistent with previous studies. Following the visual experience, the average firing rates of visual responses were reduced while the orientation and direction selectivities were increased. Light-evoked EPSCs were significantly increased for layer 5 (L5) projections to other layers of V1 after the visual experience, while the thalamocortical synaptic strength was decreased. In addition, we developed a computational model that could reproduce 5-Hz oscillations with enhanced neuronal selectivity following synaptic plasticity within the recurrent network and decreased feedforward input.SIGNIFICANCE STATEMENT Neural oscillations at around 5 Hz are involved in visual working memory and temporal expectations in primary visual cortex (V1). However, how the oscillations modulate the visual response properties of neurons in V1 and their underlying mechanism is poorly understood. Here, we show that these oscillations may alter the orientation and direction selectivity of the layer 2/3 (L2/3) neurons and correlate with the synaptic plasticity within V1. Our computational recurrent network model reproduces all these observations and provides a mechanistic framework for studying the role of 5-Hz oscillations in visual familiarity.     

Effects of corpus callosum section on functional compensation in the posteromedial lateral suprasylvian visual area after early visual cortex damage in cats

A visual cortex lesion made in adult cats leads to a loss of direction selectivity and a loss of response to the ipsilateral eye among cells in posteromedial lateral suprasylvian (PMLS) cortex of cats. However, a visual cortex lesion made in young cats results in normal direction selectivity and normal ocular dominance in PMLS cortex. Thus cats with an early lesion demonstrate functional compensation in PMLS cortex. The present experiment determined whether the functional compensation depends upon an intact corpus callosum. Cats received a unilateral visual cortex lesion on the day of birth (day 1) or at 8 weeks of age. When the cats were adult, the corpus callosum was sectioned and 24 hours later recordings were made in PMLS cortex ipsilateral to the visual cortex lesion. Results were compared to cats with a similar lesion and an intact corpus callosum. In cats with a lesion made on day 1, a corpus callosum section did not affect receptive-field properties or ocular dominance in PMLS cortex. Therefore, functional compensation is not dependent on input via the corpus callosum in these animals. However, in cats with a lesion made at 8 weeks. a corpus callosum section resulted in a decrease in the percentage of direction-selective cells and in the percentage of cells driven by the ipsilateral eye. Despite the decrease, the percentage of direction-selective cells still was greater than in cats with an adult unilateral visual cortex lesion. Thus, while partly dependent on callosal inputs, some functional compensation for direction selectivity remains on the basis of ipsilateral inputs.(ABSTRACT TRUNCATED AT 250 WORDS)     

Direction-selective patterns of activity in human visual cortex suggest common neural substrates for different types of motion

A sense of motion can be elicited by the movement of both luminance- and texture-defined patterns, what is commonly referred to as first- and second-order, respectively. Although there are differences in the perception of these two classes of motion stimuli, including differences in temporal and spatial sensitivity, it is debated whether common or separate direction-selective mechanisms are responsible for processing these two types of motion. Here, we measured direction-selective responses to luminance- and texture-defined motion in the human visual cortex by using functional MRI (fMRI) in conjunction with multivariate pattern analysis (MVPA). We found evidence of direction selectivity for both types of motion in all early visual areas (V1, V2, V3, V3A, V4, and MT+), implying that none of these early visual areas is specialized for processing a specific type of motion. More importantly, linear classifiers trained with cortical activity patterns to one type of motion (e.g., first-order motion) could reliably classify the direction of motion defined by the other type (e.g., second-order motion). Our results suggest that the direction-selective mechanisms that respond to these two types of motion share similar spatial distributions in the early visual cortex, consistent with the possibility that common mechanisms are responsible for processing both types of motion.