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Theory of orientation tuning in visual cortex.

The role of intrinsic cortical connections in processing sensory input and in generating behavioral output is poorly understood. We have examined this issue in the context of the tuning of neuronal responses in cortex to the orientation of a visual stimulus. We analytically study a simple network model that incorporates both orientation-selective input from the lateral geniculate nucleus and orientation-specific cortical interactions. Depending on the model parameters, the network exhibits orientation selectivity that originates from within the cortex, by a symmetry-breaking mechanism. In this case, the width of the orientation tuning can be sharp even if the lateral geniculate nucleus inputs are only weakly anisotropic. By using our model, several experimental consequences of this cortical mechanism of orientation tuning are derived. The tuning width is relatively independent of the contrast and angular anisotropy of the visual stimulus. The transient population response to changing of the stimulus orientation exhibits a slow "virtual rotation." Neuronal cross-correlations exhibit long time tails, the sign of which depends on the preferred orientations of the cells and the stimulus orientation.

Animals↗

Coexistence of linear zones and pinwheels within orientation maps in cat visual cortex.

Revealing the layout of cortical maps is important both for understanding the processes involved in their development and for uncovering the mechanisms underlying neural computation. The typical organization of orientation maps in the cat visual cortex is radial; complete orientation cycles are mapped around orientation singularities. In contrast, long linear zones of orientation representation have been detected in the primary visual cortex of the tree shrew. In this study, we searched for the existence of long linear sequences and wide linear zones within orientation preference maps of the cat visual cortex. Optical imaging based on intrinsic signals was used. Long linear sequences and wide linear zones of preferred orientation were occasionally detected along the border between areas 17 and 18, as well as within area 18. Adjacent zones of distinct radial and linear organizations were observed across area 18 of a single hemisphere. However, radial and linear organizations were not necessarily segregated; long (7.5 mm) linear sequences of preferred orientation were found embedded within a typical pinwheel-like organization of orientation. We conclude that, although the radial organization is dominant, perfectly linear organization may develop and perform the processing related to orientation in the cat visual cortex.

Animals↗

Orienting attention in aging and Parkinson's disease: distinguishing modes of control.

Past research on attentional orienting and Parkinson's disease (PD) has been compromised because the experimental paradigms tended to confound different forms of orienting. We sought to overcome this by examining the attentional orienting of three distinct groups (PD-patients, age-matched controls, and young controls) on five different tasks, four of which isolated pure forms of orienting. On two covert orienting tasks PD patients oriented volitional (Experiment 1) and reflexive (Experiment 2) covert attention in a healthy and normal manner for their age. On two overt orienting tasks, PD patients were found to execute volitional eye movements that were prone to undershoot their target goal (Experiment 3), and reflexive eye movements that were unusually fast (Experiment 4). When required to perform an antisaccade task (Experiment 5), which combines reflexive and volitional modes of overt orienting, PD patients performed normally. This indicates that using a task which combines different modes of orienting creates a situation that is more than the sum of its parts. Together our study supports the thesis that it is crucial to isolate and investigate different modes of attentional control.

Aged↗

Exogenous and endogenous attention orienting in autism spectrum disorders.

Fifteen children with high-functioning Autism Spectrum Disorder (ASD) and 15 children with typical development completed an attentional cuing task using peripheral cues (exogenous orienting) and central cues (endogenous orienting). Results showed that participants with ASD had impaired exogenous and intact endogenous orienting. The pattern of exogenous orienting was related to motor functioning. Individuals with ASD who had poor motor functioning displayed slowed exogenous orienting. However, individuals with ASD who had relatively good motor functioning showed typical levels of exogenous orienting when given a short time but decreased orienting when given a longer amount of time. These results suggest attention impairments in ASD may not be specific to social orienting and instead may represent a more general orienting impairment.

Adolescent↗

Relationship between orientation domains, cytochrome oxidase stripes, and intrinsic horizontal connections in squirrel monkey area V2.

Area V2, the main target of primary visual cortex projections, is characterized by a striking functional and connectional compartmentalization. Many aspects of this organization are correlated to three sets of stripes (thick, thin, and pale) revealed by cytochrome oxidase (CO) staining. Several questions related to the physiological properties of these compartments, their intrinsic connections, and points of similarity with area V1 modules are still unresolved. We have addressed some of these questions by combining the techniques of optical imaging of intrinsic signals, tract tracing, and CO histochemistry in the same patches of areas V1 and V2 of the squirrel monkey. The following observations were made. Orientation domains: in area V1 these are organized in narrow bands, while in area V2 they form patches. In area V2, domain width and distance between domains are approximately double that found in area V1. Orientation and CO stripe organization: orientation tuning was organized so that highly selective regions were centered on thick CO stripes while regions of broad orientation selectivity were centered on thin CO stripes. However, the orientation domains appeared to ignore borders between thick and pale stripes. Intrinsic connections: injections of the sensitive tracer biocytin into area V2 labeled a dense network of horizontally projecting fibers that were organized in columnar patches. Patches were small (mean width, 211 microns; mean length, 342 microns) and the labeling pattern extended over 4-5 mm. Axonal patches and CO stripes: Axonal patches found were in all three stripe compartments. However, injections that straddled the borders of thick/pale stripe compartments produced axonal projections that tended to cluster around border regions. Axonal patches and orientation domains: V2 injections produced labeling in V1 that appeared to be organized in narrow bands, reminiscent of orientation domain distribution in V1. Within area V2, axonal patches targeted a wide range of orientation domains, but appeared to avoid domains having orthogonal orientation preference to that found at the injection site. To conclude, our results show, on the one hand, a measure of functional specificity for the CO stripes and the intrinsic connections. On the other hand, they indicate additional substructures within area V2, whose precise relationship to the known compartmental organization remains to be clarified.

Animals↗

Orientation and direction selectivity of neurons in V1 of alert monkeys: functional relationships and laminar distributions.

We studied orientation selectivity in V1 of alert monkeys and its relationship to other physiological parameters and to anatomical organization. Single neurons were stimulated with drifting bars or with sinusoidal gratings while compensating for eye position. Orientation selectivity based on spike counts was quantified by circular variance and by the bandwidth of the orientation tuning curve. The circular variance distribution was bimodal, suggesting groups with low and with high selectivity. Orientation selectivity was clearly correlated with spontaneous activity, classical receptive field (CRF) size and the strength of surround suppression. Laminar distributions of neuronal properties were distinct. Neurons in the output layers 2/3, 4B and 5 had low spontaneous activity, small CRFs and high orientation selectivity, while the input layers had greater diversity. Direction-selective cells were among the neurons most selective for orientation and most had small CRFs. A narrow band of direction- and orientation-selective cells with small CRFs was located in the middle of layer 4C, indicating appearance of very selective cells at an early stage of cortical processing. We suggest that these results reflect interactions between excitatory and inhibitory mechanisms specific to each sublamina. Regions with less inhibition have higher spontaneous activity, larger CRFs and broader orientation tuning. Where inhibition is stronger, spontaneous activity almost disappears, CRFs shrink, and orientation selectivity is high.

Action Potentials↗

Covert and overt orienting to gaze direction cues and the effects of fixation offset.

We examined covert and overt orienting in response to non-predictive gaze direction cues and investigated whether the subcortical superior colliculus (SC) plays a role in this type of orienting. Participants viewed a centrally presented gazing schematic face and responded to targets appearing at gazed-at or non-gazed-at locations either by making a keypress response while maintaining central fixation or by making an eye movement to the target. For both response conditions, the fixation stimulus (the gazing face) either remained on the screen or was extinguished at the time of target presentation, a manipulation known to engage and disengage the SC. Results revealed that participants making manual responses oriented covertly to the gazed-at location regardless of the fixation condition, and that participants making eye movements oriented overtly only if the fixation stimulus remained on the screen. Overt gaze-triggered orienting was not enhanced relative to covert orienting, and the fixation offset effect was not reduced for averted gaze cues relative to straight gaze cues. These findings suggest that gaze direction cues do not activate or predisengage the oculomotor system, and thus that orienting to gaze direction does not engage the SC. This is consistent with the view that gaze-triggered orienting is a unique form of reflexive orienting that depends crucially on cortical processes.

Adult↗

Spatial frequency tuning of orientation-discontinuity-sensitive corticofugal feedback to the cat lateral geniculate nucleus.

1. The influence of spatial frequency on the inhibitory component of the effects mediated by feedback from the visual cortex has been examined in X and Y cells in the A laminae of the feline dorsal lateral geniculate nucleus (dLGN). Experiments utilized a concentric, bipartite visual stimulus centered over the receptive fields of the cells studied. The responses of dLGN cells to selective stimulation of receptive field centre (with the inner window) were compared with those to stimulation of centre and surround mechanisms (both inner and outer window), with the stimuli either in or out of orientation alignment. 2. With these same stimuli, layer VI cells in the visual cortex showed a marked increase in response magnitude when the inner and outer components of the stimulus were in orientation alignment, and presented at the preferred orientation. In the case of dLGN X and Y cells we observed an enhancement of the surround antagonism of the centre response when the inner and outer sections of the stimulus were in orientation alignment. 3. The effects of varying spatial frequency on these responses were examined in dLGN cells in the presence of corticofugal feedback. With the stimulus sections in orientation alignment, surround stimulation produced a powerful and significant reduction in the response to stimulation of centre mechanism alone with the most marked effects for stimuli in the range 0.1-0.85 cycles per degree (c.p.d.). The reduction produced by surround stimulation in the range 0.1-0.5 c.p.d. was notably more potent in X cells than in Y cells. 4. The responses to the same stimuli were examined in dLGN cells with the corticofugal feedback inactivated. Comparison of data from cells studied with and without feedback revealed a significant decrease in surround-mediated attenuation of the centre response in Y cells for spatial frequencies in the range 0.1-0.85 c.p.d. For X cells the decrease in strength of the surround antagonism was also clear and significant but only seen in the range 0.1-0.5 c.p.d. 5. The influence of the orientation alignment of inner and outer stimulus sections revealed a marked difference between cells studied with and without feedback. In the presence of feedback fully aligned stimuli enhanced surround antagonism of centre responses for spatial frequencies in the range 0.1-0.5 c.p.d., in X and Y cells. In the absence of corticofugal feedback this alignment effect was essentially eliminated. 6. These data show that surround antagonism of the centre response is influenced by orientation alignment of the stimulus sections at low spatial frequencies and in the presence of corticofugal feedback. They support a cortically driven enhancement of the inhibitory mechanisms reinforcing surround mechanisms in the dLGN. We propose that feedback enhances a low spatial frequency cut-off in the dLGN, that this effect is maximal for a continuous iso-orientated contour, but diminished whenever there is an orientation discontinuity. The hyperpolarizing influence underlying this effect may contribute to the recently described synchronizing influence of the direct corticofugal contacts onto relay cells. We suggest feedback of the cortical level of analysis refines the transfer of the visual input at geniculate level in a stimulus-context-dependent fashion.

Animals↗

Comparison among some models of orientation selectivity.

Several models exist for explaining primary visual cortex (V1) orientation tuning. The modified feedforward model (MFM) and the recurrent model (RM) are major examples. We have implemented these two models, at the same level of detail, alongside a few newer variations, and thoroughly compared their receptive-field structures. We found that antiphase inhibition in the MFM enhances both spatial phase information and orientation tuning, producing well-tuned simple cells. This remains true for a newer version of the MFM that incorporates untuned complex-cell inhibition. In contrast, when the recurrent connections in the RM are strong enough to produce typical V1 orientation tuning, they also eliminate spatial phase information, making the cells complex. Introducing phase specificity into the connections of the RM (as done in an original version of the RM) can make the cells phase sensitive, but the cells show an incorrect 90 degrees peak shift of orientation tuning under opposite contrast signs. An inhibition-dominant version of the RM can generate well-tuned cells across the simple-complex spectrum, but it predicts that the net effect of cortical interactions is to suppress feedforward excitation across all orientations in simple cells. Finally, adding antiphase inhibition used in the MFM into the RM produces a most general model. We call this new model the modified recurrent model (MRM) and show that this model can also produce well-tuned cells throughout the simple-complex spectrum. Unlike the inhibition-dominant RM, the MRM is consistent with data from cat V1, suggesting that the net effect of cortical interactions is to boost simple cell responses at the preferred orientation. These results suggest that the MFM is well suited for explaining orientation tuning in simple cells, whereas the standard RM is for complex cells. The assignment of the RM to complex cells also avoids conflicts between the RM and the experiments of cortical inactivation (done on simple cells) and the spatial-frequency dependency of orientation tuning (found in simple cells). Because orientation-tuned V1 cells show a continuum of simple- to complex-cell behavior, the MRM provides the best description of V1 data.

Animals↗

The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior.

We have compared the effects of contrast on human psychophysical orientation and spatial frequency discrimination thresholds and on the responses of individual neurons in the cat's striate cortex. Contrast has similar effects on orientation and spatial frequency discrimination: as contrast is increased above detection threshold, orientation and spatial frequency discrimination performance improves but reaches maximum levels at quite low contrasts. Further increases in contrast produce no further improvements in discrimination. We measured the effects of contrast on response amplitude, orientation and spatial frequency selectivity, and response variance of neurons in the cat's striate cortex. Orientation and spatial frequency selectivity vary little with contrast. Also, the ratio of response variance to response mean is unaffected by contrast. Although, in many cells, response amplitude increases approximately linearly with log contrast over most of the visible range, some cells show complete or partial saturation of response amplitude at medium contrasts. Therefore, some cells show a clear increase in slope of the orientation and spatial frequency tuning functions with increasing contrast, whereas in others the slopes reach maximum values at medium contrasts. Using receiver operating characteristic analysis, we estimated the minimum orientation and spatial frequency differences that can be signaled reliably as a response change by an individual cell. This analysis shows that, on average, the discrimination of orientation or spatial frequency improves with contrast at low contrasts more than at higher contrasts. Using the optimal stimulus for each cell, we estimated the contrast threshold of 48 neurons. Most cells had contrast thresholds below 5%. Thresholds were only slightly higher for nonoptimal stimuli. Therefore, increasing the contrast of sinusoidal gratings above approximately 10% will not produce large increases in the number of responding cells. The observed effects of contrast on the response characteristics of nonsaturating cortical cells do not appear consistent with the psychophysical results. Cells that reach their maximum response at low-to-medium contrasts may account for the contrast independence of psychophysical orientation and spatial frequency discrimination thresholds at medium and high contrasts.

Animals↗

Organization of orientation and direction selectivity in areas 17 and 18 of cat cerebral cortex.

1. The organization of subunits and sequences subserving preferred stimulus orientation and preferred direction of stimulus motion in cat cerebral cortical areas 17 and 18 was determined by making vertical, tangential, and oblique microelectrode penetrations into those areas. 2. Quantitative measurements of direction selectivity indicated that not all shades of direction selectivity are equally represented in area 17. Peaks in the distribution of direction indices may correspond to the bidirectional, direction biased, and direction selective categories used in qualitative studies. 3. The relationship between preferred direction and location in the visual field was examined for units with receptive fields centered more than 15 degrees from the area centralis. Simple cells had orientation preferences that tended to be parallel to radii extending out from the area centralis. Wide-field complex cells had orientation preferences that tended to be parallel to concentric circles centered on the area centralis; the direction preferences of this group were biased toward motion away from the area centralis. 4. Unit pairs separated by 200 microns or less were 4.2 times as likely to have the same preferred direction as to have opposite preferred directions, indicating that, on average, strings of five neurons have similar direction preferences. 5. Tracks in area 18 showed a similar pattern to those in area 17. 6. In the vertical tracks in area 17 a small proportion (12%) of the units recorded in infragranular layers had preferred orientations that deviated 30 degrees or more from the first unit recorded in the same column. The presence of these cells most likely reflects the relative crowding of columns in infragranular layers, which occurs at the crown of the lateral gyrus. Columns with such large jumps in preferred orientation were not observed in area 18, which occupies a relatively flat region of cortex. 7. In both areas 17 and 18 direction preference in vertical tracks usually reversed at least once, either between supra- and infragranular layers or within infragranular layers. Along these same tracks, orientation preference usually did not change. 8. In tangential tracks, preferred direction and orientation preferences changed together in small increments. Occasionally a large jump in preferred direction would occur with only a small change in preferred orientation. These large jumps were considered to mark the boundaries of the direction sequences. Most frequently these boundaries were separated by 400-600 microns. This value is approximately half the size of a complete set of orientation preferences (700-1,200 microns).(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex.

In the primary visual cortex of monkey and cat, ocular dominance and orientation are represented continuously and simultaneously, so that most neighboring neurons respond optimally to visual stimulation of the same eye and orientation. Maps of stimulus orientation are punctuated by singularities referred to as "pinwheel centers," around which all orientations are represented. Given that the orientation map is mostly continuous, orientation singularities are a mathematical necessity unless the map consists of perfectly parallel rows, and there is no evidence that the singularities play a role in normal function or development. We report here that in cats there is a strong tendency for peaks of ocular dominance to lie on the pinwheel center singularities of the orientation map. This relationship predicts but is not predicted by the tendencies, previously reported, for pinwheels to lie near the center lines of ocular dominance bands and for iso-orientation bands to cross ocular dominance boundaries at right angles. The coincidence of ocular dominance peaks with orientation singularities is likely to reflect a strong underlying functional link between the two visual cortical maps.

Animals↗

Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors.

The peripheral neural representation of object shape and orientation was studied by recording the responses of a spatially distributed population of rapidly and slowly adapting type I mechanoreceptors (RAs and SAs, respectively) to objects of different shapes and orientations indented at a fixed location on the fingerpad of the anesthetized monkey. The toroidal objects had a radius of 5 mm on the major axis, and 1, 3, or 5 mm on the minor axis. Each object was indented into the fingerpad for 4 s at orientations of 0, 45, 90, and 135 degrees using a contact force of 15 gwt. Estimations of the population responses (PRs) were constructed by combining the responses of 91 SA and 97 RA single afferents at discrete times during the indentation. The PR was composed of the neural discharge rates (z coordinate) plotted at x and y coordinates of the most sensitive spot of the receptive field. The shapes of the PRs were related to the shapes of the objects by fitting the PRs with Gaussian surfaces. The orientations of the PRs were determined from weighted principal component analyses. The SA PR encoded both the orientation and shape of the objects, whereas the RA PR did neither. The SA PR orientation was biased toward the long axis of the finger. The RA PR encoded orientation only for the object with the highest curvature but did so ambiguously. Only the SA PR was well fit by a Gaussian surface. The shape of the object was discriminated by the SA PR within the first 500 ms of contact, and the form of the SA PR remained constant during the subsequent 3.5 s. This was manifested by constant widths of the PR along the major and minor axes despite a peak response that decreased from its maximum at 200 ms to an asymptotic value starting at 1 s. Thus the shape and orientation of each object were coded by the shape and orientation of the SA PR.

Adaptation, Physiological↗

Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex.

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20-300%, generally more in simple cells (40-300%) than in complex cells (20-120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.

Action Potentials↗

Impaired orientation in acute stroke: frequency, determinants, and time-course of recovery. The Copenhagen Stroke Study.

Orientation is an indicator of general intellectual function and is defined as the ability to report time, place, and personal data. Our knowledge of orientation in acute stroke is sparse. We examined the frequency of impaired orientation in acute stroke, its determinants, and recovery in 653 consecutive patients with acute stroke who were not unconscious and who were without severe aphasia. Prospective assessments of orientation and stroke severity were done by the Scandinavian Neurologic Stroke Scale at the time of acute admission and hereafter weekly until the end of rehabilitation. Impaired orientation was found in 23% of the patients on acute admission and in 12% of the survivors after completed rehabilitation. A stationary level of orientation was achieved by 80% of the patients within 2 weeks and by 95% within 6 weeks. A multiple linear regression analysis found neurological score (B = 0.027, SE(B) = 0.003), age (B = -0.013, SE(B) = 0.003), and comorbidity (B = -0.023, SE(B) = 0.078), but not sex, prior stroke, handedness, or side of stroke lesion to be significant independent determinants of orientation score on acute admission. Lesions involving the anterior and medial thalamus and/or any of the cerebral lobes were associated with impaired orientation. In conclusion, impaired orientation is frequent in acute stroke and the time-course of recovery is similar to what has been found in other neuropsychological impairments with the major part of recovery early after stroke onset.

Acute Disease↗

Expectancy of line segment orientation.

The question was asked whether briefly flashed line segments are easier to detect when presented at an expected, rather than an unexpected, orientation. Detection rates were measured in a two-interval forced choice (2IFC) paradigm that did not require the subject to identify the orientation of the line segment, only to detect its presence. The 2IFC paradigm was used to rule out bias or criterion effects. Subjects were led to expect lines in a particular or primary orientation by being presented lines with that orientation as cues before every trial, and by being tested with only that orientation during practice. Lines of the orthogonal, probe orientation replaced the primary on 25% of experimental trials. When the stimulus location was known in advance, lines of the primary orientation were detected more accurately than were probe lines, but when stimulus location was not known, detection rates were equal. Detection rates were also equal when subjects were informed of the probe at the end of the practice period, so that both orientations were expected; hence the subjects' expectations, not the probability of stimulus occurrence, are necessary for the effect to occur. Thus expecting a line of a particular orientation at a particular location facilities its detection.

Form Perception↗

Involuntary attentional shifts due to orientation differences.

We tested the ability of orientation differences to cause involuntary shifts of visual attention and found that these attentional shifts can occur in response to an orientation "pop-out" display. Texture-like cue stimuli consisting of discrete oriented bars, with either uniform orientation or containing a noninformative orthogonally oriented bar, were presented for a variable duration. Subsequent to or partially coincident with the cue stimulus was the target display of a localization or two-interval forced-choice task, followed by a mask display. Naive subjects consistently showed greater accuracy in trials with the target at the location of the orthogonal orientation compared with trials with uniformly oriented bars, with only 100 msec between the cue and mask onsets. Discriminating these orientations required a stimulus onset asynchrony (SOA) of 50-70 msec. The attentional facilitation is transient, in most cases absent with a cue-mask SOA of 250 msec [corrected]. These results suggest that the preattentive character of some texture discrimination tasks with SOAs of only 100 msec is vitiated by the involuntary attentional shifts that are caused by orientation differences.

Adolescent↗

Orientation invariance in naming rotated objects: individual differences and repetition priming.

In naming drawings of complex common objects, unpracticed naming times increase with rotation away from the upright, but this orientation effect is attenuated with practice. In principle, attenuation could result from learning to extract orientation-invariant information or from learning view-specific representations at the trained orientations. We contrasted these approaches by examining repetition priming for prime-target pairs presented on successive trials in either the same orientation (horse at 51 degrees primes horse at 51 degrees) or a different orientation (horse at 154 degrees primes horse at 51 degrees), for two subgroups of subjects. One subgroup showed no orientation effect, even when unpracticed, and a correspondingly high generalization of priming across different views. The other subgroup initially showed high sensitivity to misorientation and little priming across orientations but, with sufficient practice, came to show no orientation effect and complete generalization of priming. Thus, some subjects always used orientation-invariant procedures, whereas others learned to do so.

Adult↗