Two spatially separated attention systems in the visual field: evidence from inhibition of return

It has been demonstrated that the human visual field shows some functional inhomogeneities, in particular when the central and perifoveal regions are compared to the more peripheral regions. The present study examined this inhomogeneity by examining the effect of stimulus eccentricity on inhibition of return (IOR), a phenomenon that biases our attention towards novel locations against returning it back to previously attended locations. Eighteen subjects were examined in a visual detection task, in which a target appeared randomly following a nonpredictive spatial cue in the visual field. The eccentricities of the cues and targets were systematically manipulated from 5° to 30° with 5° increments. Results showed that response times to targets that appeared at cued locations were significantly slower than those at uncued locations for all stimulus eccentricities, demonstrating the IOR effects. However, response times at cued locations increased significantly when stimulus eccentricity shifted from 15° to 20°, leading to a much stronger IOR effect at more peripheral regions compared to central and perifoveal regions, indicating a functional dissociation between these two regions of the visual field. Possible neural mechanisms underlying this dissociation are discussed, and two attention systems modulating the two functional regions of the visual field are put forward to best account the present finding implicating in particular midbrain mechanism.     

Spatial orienting in the visual field: a unified perceptual space?

Visual attention can be oriented toward a spatial location in the visual field exogenously by an abrupt onset of a peripheral cue. In a series of behavioral studies on exogenous orienting of attention with a double-cue paradigm, we demonstrated a functional subdivision of perceptual space in the visual field. Specifically, inhibition of return (IOR) is much stronger at periphery relative to perifoveal visual field up to approximately 15° eccentricity, suggesting two dissociable functional areas in the visual field. To further investigate the generality of this functional subdivision of the visual field, we measured IOR effects with another single-cue paradigm and applied a very short cue-target interval that was typically anticipated not to observe any inhibitory effect at all. Consistent with this expectation, no IOR effects at the eccentricities up to 15° were observed. However, significant IOR effects beyond 15° eccentricities were consistently demonstrated. These results not only revealed an early onset of IOR for more peripheral stimuli, but also confirmed that the perceptual space in the visual field is not homogeneous but underlies a functional subdivision with a border of ca. 15° eccentricity.     

Spatial orienting in the visual field: a unified perceptual space?

Visual attention can be oriented toward a spatial location in the visual field exogenously by an abrupt onset of a peripheral cue. In a series of behavioral studies on exogenous orienting of attention with a double-cue paradigm, we demonstrated a functional subdivision of perceptual space in the visual field. Specifically, inhibition of return (IOR) is much stronger at periphery relative to perifoveal visual field up to approximately 15° eccentricity, suggesting two dissociable functional areas in the visual field. To further investigate the generality of this functional subdivision of the visual field, we measured IOR effects with another single-cue paradigm and applied a very short cue-target interval that was typically anticipated not to observe any inhibitory effect at all. Consistent with this expectation, no IOR effects at the eccentricities up to 15° were observed. However, significant IOR effects beyond 15° eccentricities were consistently demonstrated. These results not only revealed an early onset of IOR for more peripheral stimuli, but also confirmed that the perceptual space in the visual field is not homogeneous but underlies a functional subdivision with a border of ca. 15° eccentricity.     

三维空间中不同视野深度位置上的返回抑制

通过虚拟现实构建虚拟三维场景,将二维平面视觉空间返回抑制范式应用到三维空间,通过两个实验操纵了目标深度、线索有效性以及视野位置三个变量,考察注意在三维空间不同视野深度位置上进行定向/重定向产生的返回抑制效应。结果发现,(1)二次线索化位于固定的中央视野时,不论目标出现在近处空间还是出现在远处空间,外周视野条件下的返回抑制大于中央视野条件下的返回抑制;(2)二次线索化位于非固定的中央视野时,近处空间和远处空间的返回抑制存在分离,表现为当目标出现在远处空间时,外周视野条件下的返回抑制效应减小。研究表明,三维空间中外周视野深度位置上的返回抑制与中央视野深度位置上的返回抑制存在差异。     

Inhibition of return in subliminal letter priming

The present study combined exogenous spatial cueing with masked repetition priming to study attentional influences on the processing of subliminal stimuli. Participants performed an alphabetic decision task (letter versus pseudo-letter classification) with central targets and briefly presented peripherally located primes that were either cued or not cued by an abrupt onset. A relatively long delay between cue and prime was used to investigate the effect of inhibition of return (IOR) on the processing of subliminal masked primes. Primes presented to the left visual field showed standard effects of Cue Validity and no IOR (significant priming with valid cues only). Primes presented to the right visual field showed no priming from valid cues (an IOR effect), and priming with invalid cues that depended on hand of response to letter targets (right-hand in Experiment 1, left-hand in Experiment 2). The results are interpreted in terms of a differential speed of engagement and disengagement of attention to the right and left visual fields for alphabetic stimuli, coupled with a complex interaction that arises between Prime Relatedness and response-hand.     

Developmental trajectory of neural specialization for letter and number visual processing

Adult neuroimaging studies have demonstrated dissociable neural activation patterns in the visual cortex in response to letters (Latin alphabet) and numbers (Arabic numerals), which suggest a strong experiential influence of reading and mathematics on the human visual system. Here, developmental trajectories in the event‐related potential (ERP) patterns evoked by visual processing of letters, numbers, and false fonts were examined in four different age groups (7‐, 10‐, 15‐year‐olds, and young adults). The 15‐year‐olds and adults showed greater neural sensitivity to letters over numbers in the left visual cortex and the reverse pattern in the right visual cortex, extending previous findings in adults to teenagers. In marked contrast, 7‐ and 10‐year‐olds did not show this dissociable neural pattern. Furthermore, the contrast of familiar stimuli (letters or numbers) versus unfamiliar ones (false fonts) showed stark ERP differences between the younger (7‐ and 10‐year‐olds) and the older (15‐year‐olds and adults) participants. These results suggest that both coarse (familiar versus unfamiliar) and fine (letters versus numbers) tuning for letters and numbers continue throughout childhood and early adolescence, demonstrating a profound impact of uniquely human cultural inventions on visual cognition and its development.     

Inhibition of return generated by voluntary saccades is independent of attentional momentum

Summoning attention to a peripheral location, either by a peripheral cue with the eyes fixed or when a voluntary saccade is made to it and gaze is then returned to the centre, delays detection of subsequent targets at that location compared to a location in the opposite visual field. It has been proposed that oculomotor activation generates this inhibition of return (IOR). This account presupposes that the asymmetry in detection results from inhibition at the cued location rather than facilitation at the uncued location. This has been confirmed for exogenously generated IOR. However, it has not, heretofore, been confirmed for “IOR” generated by voluntary saccades. The current study investigated whether the asymmetry in target detection, elicited either by a peripheral flash or by an eye movement generated in response to a central arrowhead, reflects facilitation at the opposite location due to the path of attentional momentum. Reaction times at the cued location were slower than reaction times at the opposite or perpendicular locations, which did not differ. Opposite facilitation due to attentional momentum requires that opposite be faster than perpendicular, which was not obtained. The results were the same whether IOR was generated by an exogenous cue or by a saccade executed endogenously to a central arrow.     

Inhibition of return

Immediately following an event at a peripheral location there is facilitation for the processing of other stimuli near that location. This is said to reflect a reflexive shift of attention towards the source of stimulation. After attention is removed from such a peripheral location, there is then delayed responding to stimuli subsequently displayed there. This inhibitory aftereffect, first described in 1984 and later labeled 'inhibition of return (IOR)', encourages orienting towards novel locations and hence might facilitate foraging and other search behaviors. Since its relatively recent discovery, IOR has been the subject of intensive investigation, from many angles and with a wide variety of approaches. After describing the seminal contribution of Posner and Cohen ('Who'), this review will discuss what causes IOR and, once initiated, what effects IOR has on subsequent processing ('What'). The time course ('When') and spatial distribution ('Where') of IOR, and what is known about IOR's neural implementation ('How') and functional significance ('Why') are also discussed.     

Visual and motor effects in inhibition of return

Inhibition of return (IOR) refers to slowed reaction times (RTs) when a target appears in the same rather than a different location as a preceding stimulus. The present study tested the hypothesis that IOR reflects a motor bias rather than a perceptual deficit. Two signals (S1 and S2) were presented on each trial. These signals were peripheral onsets or central arrows. The responses required to S1 and S2 were, respectively, no response-manual, manual-manual, saccadic-manual, no response-saccadic, manual-saccadic, and saccadic-saccadic. Uniting perceptual and motor bias views of IOR, the results demonstrated inhibition for responding to (a) peripheral signals when the eyes remained fixed (slowed visual processing) and (b) both peripheral and central signals when the eyes moved (slowed motor production). However, the results also emphasized that the nature of IOR depends fundamentally on the response modality used to reveal its influence.     

Inhibition of return and repetition priming effects in localization and discrimination tasks.

Inhibition of return (IOR) refers to slower responding to a stimulus that is presented at the same, rather than a different location as a preceding, spatially nonpredictive, stimulus. Repetition priming refers to speeded responding to a stimulus that duplicates the visual characteristics of a stimulus that precedes it. IOR and repetition priming effects interact in nonspatial discrimination tasks but not in localization tasks; three experiments examined whether this is due to processing differences or due to response differences between tasks. Two stimuli, S1 and S2, occurred on each trial. In Experiment 1, S1 and S2 were both peripheral arrows; in Experiment 2, S1 was a central arrow and S2 was a peripheral nondirectional rectangle; in Experiment 3, S1 was a peripheral nondirectional rectangle and S2 was a peripheral arrow. S1 never required a response; S2 required a localization or a discrimination response. Despite evidence that form information was likely extracted from the arrow stimuli, the localization task revealed no repetition priming: IOR occurred regardless of shared visual identity of the S1 and S2 arrows. The discrimination task revealed IOR only when the visual identity changed from S1 to S2; otherwise, facilitation occurred. These results suggest that IOR is masked by repetition priming only when the response depends on the explicit processing of form information; repetition priming does not occur when such information is extracted automatically but is task (and response) irrelevant.     

Sensori‐motor experience leads to changes in visual processing in the developing brain

Since Broca’s studies on language processing, cortical functional specialization has been considered to be integral to efficient neural processing. A fundamental question in cognitive neuroscience concerns the type of learning that is required for functional specialization to develop. To address this issue with respect to the development of neural specialization for letters, we used functional magnetic resonance imaging (fMRI) to compare brain activation patterns in pre‐school children before and after different letter‐learning conditions: a sensori‐motor group practised printing letters during the learning phase, while the control group practised visual recognition. Results demonstrated an overall left‐hemisphere bias for processing letters in these pre‐literate participants, but, more interestingly, showed enhanced blood oxygen‐level‐dependent activation in the visual association cortex during letter perception only after sensori‐motor (printing) learning. It is concluded that sensori‐motor experience augments processing in the visual system of pre‐school children. The change of activation in these neural circuits provides important evidence that ‘learning‐by‐doing’ can lay the foundation for, and potentially strengthen, the neural systems used for visual letter recognition.     

Tracking the influence of reflexive attention on sensory and cognitive processing

Previously, we demonstrated that reflexive attention facilitates early visual processing during form discrimination (Hopfinger & Mangun, 1998). In the present study, we tested whether reflexive facilitation of early visual processing will be generated when task load is low (simple luminance detection). Target stimuli that were preceded at short cue-to-target intervals by irrelevant visual events (cues) elicited an enhanced sensory (P1) event-related potential (ERP) component as well as an enhanced longer latency, cognitive ERP component (P300). At long cue-to-target intervals, facilitation in these ERP components was no longer observed, and, although inhibition of return (IOR) was observed in reaction times, the ERPs did not show an inhibition of sensory processing. These results provide converging evidence that reflexive attention transiently facilitates neural processing of visual inputs at multiple stages of analysis (i.e., sensory processing and higher order cognitive processing) but question the view that IOR is manifest at the earliest visual cortical stages of analysis.     

Neural correlates of rumination in adolescents with remitted major depressive disorder and healthy controls

The aim of the present study was to use fMRI to examine the neural correlates of engaging in rumination among a sample of remitted depressed adolescents, a population at high risk for future depressive relapse. A rumination induction task was used to assess differences in the patterns of neural activation during rumination versus a distraction condition among 26 adolescents in remission from major depressive disorder (rMDD) and in 15 healthy control adolescents. Self-report depression and rumination, as well as clinician-rated depression, were also assessed among all participants. All of the participants recruited regions in the default mode network (DMN), including the posterior cingulate cortex, medial prefrontal cortex, inferior parietal lobe, and medial temporal gyrus, during rumination. Increased activation in these regions during rumination was correlated with increased self-report rumination and symptoms of depression across all participants. Adolescents with rMDD also exhibited greater activation in regions involved in visual, somatosensory, and emotion processing than did healthy peers. The present findings suggest that during ruminative thought, adolescents with rMDD are characterized by increased recruitment of regions within the DMN and in areas involved in visual, somatosensory, and emotion processing.     

Domain-dependent activation during spatial and nonspatial auditory working memory

Visual system has been proposed to be divided into two, the ventral and dorsal, processing streams. The ventral pathway is thought to be involved in object identification whereas the dorsal pathway processes information regarding the spatial locations of objects and the spatial relationships among objects. Several studies on working memory (WM) processing have further suggested that there is a dissociable domain-dependent functional organization within the prefrontal cortex for processing of spatial and nonspatial visual information. Also the auditory system is proposed to be organized into two domain-specific processing streams, similar to that seen in the visual system. Recent studies on auditory WM have further suggested that maintenance of nonspatial and spatial auditory information activates a distributed neural network including temporal, parietal, and frontal regions but the magnitude of activation within these activated areas shows a different functional topography depending on the type of information being maintained. The dorsal prefrontal cortex, specifically an area of the superior frontal sulcus (SFS), has been shown to exhibit greater activity for spatial than for nonspatial auditory tasks. Conversely, ventral frontal regions have been shown to be more recruited by nonspatial than by spatial auditory tasks. It has also been shown that the magnitude of this dissociation is dependent on the cognitive operations required during WM processing. Moreover, there is evidence that within the nonspatial domain in the ventral prefrontal cortex, there is an across-modality dissociation during maintenance of visual and auditory information. Taken together, human neuroimaging results on both visual and auditory sensory systems support the idea that the prefrontal cortex is organized according to the type of information being maintained in WM.     

Inhibition of return exaggerates change blindness

Peripheral cues trigger attention shifts, which facilitate perceptual processing and enhance visual awareness. However, this facilitation is superseded by an inhibition of return (IOR) effect, which biases attention away from the cued location. While the link between facilitatory effects of visual attention and awareness is well established, no study has reported negative effects of spatial cueing on visual awareness. This failure is puzzling, given the claim that attention is a necessary precondition for awareness. If attention is necessary for awareness, inhibiting attention should also inhibit awareness. This leads to a slightly counterintuitive prediction: Spatial cueing will inhibit awareness at long cue–target latencies. This study shows that subliminal peripheral cues exaggerate change blindness at long cue–change latencies, demonstrating that IOR can suppress visual awareness of changes and suggesting that IOR can directly affect the contents of consciousness.     

Neural adaptation across viewpoint and exemplar in fusiform cortex

The visual system has the remarkable ability to generalize across different viewpoints and exemplars to recognize abstract categories of objects, and to discriminate between different viewpoints and exemplars to recognize specific instances of particular objects. Behavioral experiments indicate the critical role of the right hemisphere in specific-viewpoint and -exemplar visual form processing and the left hemisphere in abstract-viewpoint and -exemplar visual form processing. Neuroimaging studies indicate the role of fusiform cortex in these processes, however results conflict in their support of the behavioral findings. We investigated this inconsistency in the present study by examining adaptation across viewpoint and exemplar changes in the functionally defined fusiform face area (FFA) and in fusiform regions exhibiting adaptation. Subjects were adapted to particular views of common objects and then tested with objects appearing in four critical conditions: same-exemplar, same-viewpoint adapted, same-exemplar, different-viewpoint adapted, different-exemplar adapted, and not adapted. In line with previous results, the FFA demonstrated a release from neural adaptation for repeated different viewpoints and exemplars of an object. In contrast to previous work, a (non-FFA) right medial fusiform area also demonstrated a release from neural adaptation for repeated different viewpoints and exemplars of an object. Finally, a left lateral fusiform area demonstrated neural adaptation for repeated different viewpoints, but not exemplars, of an object. Test-phase task demands did not affect adaptation in these regions. Together, results suggest that dissociable neural subsystems in fusiform cortex support the specific identification of a particular object and the abstract recognition of that object observed from a different viewpoint. In addition, results suggest that areas within fusiform cortex do not support abstract recognition of different exemplars of objects within a category.     

Cognitive and neuronal processes involved in sequential generation of general and specific mental images

Mental image generation is a complex process mediated by dynamically interrelated components, e.g. image generation and image enrichment of details. This study investigated the cognitive and neural correlates of sequential image generation. An event-related fMRI experiment was carried out in which general and specific images had to be generated sequentially in two different positions. Participants had to generate either a general image first and then a specific one or a specific image first and then a general one, in response to the same word-stimulus. Generation times showed that specific images took shorter to be produced if they had been preceded by the generation of a general image. The fMRI results showed that position of generation and type of image was associated with different patterns of neurofunctional change. When an image was generated as first, areas of activation were found in the parahippocampal, fusiform and occipital regions. These are areas associated with memory retrieval and visual processing. When an image was generated as second, significant activations were found in superior temporal and precuneus areas, brain structures that are involved in the storage of visual memory for object shapes and imagery, respectively. The generation of a general image was supported by frontal areas and by the precuneus. The generation of a specific image involved frontal and thalamic areas (structures associated with visual processing of details) and the posterior cingulate cortex. When shifting from a specific image to a general one, a higher level of activity was found in the middle frontal gyrus involved in global visuo-spatial processing, suggesting that the generation of specific images required the retrieval of an object’s global shape. Altogether, these data suggest that the sequential generation of different types of image is associated with discrete processes but also shares common cognitive and neural components.     

Inhibition of return in manual and saccadic response systems

When nonpredictive exogenous visual cues are used to reflexively orient covert visual spatial attention, the initial early facilitation for detecting stimuli at cued versus uncued spatial locations develops into inhibition by 300 msec following the cue, a pattern referred to as inhibition of return (IOR). Experiments were carried out comparing the magnitude and time course for development of IOR effects when manual versus saccadic responses were required. The results showed that both manual and saccadic responses result in equivalent amounts of facilitation following initial exposure to a spatial cue. However, IOR developed more quickly for saccadic responses, such that, at certain cue-target SOAs, saccadic responses to targets were inhibited, whereas manual responses were still facilitated. The findings are interpreted in terms of a premotor theory of visual attention.     

Linking patterns of infant eye movements to a neural network model of the ventral stream using representational similarity analysis

Little is known about the development of higher-level areas of visual cortex during infancy, and even less is known about how the development of visually guided behavior is related to the different levels of the cortical processing hierarchy. As a first step toward filling these gaps, we used representational similarity analysis (RSA) to assess links between gaze patterns and a neural network model that captures key properties of the ventral visual processing stream. We recorded the eye movements of 4- to 12-month-old infants (N = 54) as they viewed photographs of scenes. For each infant, we calculated the similarity of the gaze patterns for each pair of photographs. We also analyzed the images using a convolutional neural network model in which the successive layers correspond approximately to the sequence of areas along the ventral stream. For each layer of the network, we calculated the similarity of the activation patterns for each pair of photographs, which was then compared with the infant gaze data. We found that the network layers corresponding to lower-level areas of visual cortex accounted for gaze patterns better in younger infants than in older infants, whereas the network layers corresponding to higher-level areas of visual cortex accounted for gaze patterns better in older infants than in younger infants. Thus, between 4 and 12 months, gaze becomes increasingly controlled by more abstract, higher-level representations. These results also demonstrate the feasibility of using RSA to link infant gaze behavior to neural network models. A video abstract of this article can be viewed at https://youtu.be/K5mF2Rw98Is     

视觉意识及其神经机制

视觉意识的神经机制是当前认知神经科学研究的热点问题之一。过去普遍认为视觉信息加工主要有两条通路:腹侧通路和背侧通路;而新近的研究表明还存在不经过初级视觉皮层(V1区)的第三条通路。高级视觉皮层、V1区和皮层下结构都对意识觉知的产生起到了相应的作用。已有的实验证据表明,意识的产生过程异常复杂,仍有很多问题值得继续深入讨论和研究。