Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus.

The primate posterior parietal cortex (PPC) plays an important role in representing and recalling spatial relationships and in the ability to orient visual attention. This is evidenced by the parietal activation observed in brain imaging experiments performed during visuo- spatial tasks, and by the contralateral neglect syndrome that often accompanies parietal lesions. Individual neurons in monkey parietal cortex respond vigorously to the appearance of single, behaviorally relevant stimuli, but little is known about how they respond to more complex visual displays. The current experiments addressed this issue by recording activity from single neurons in area 7a of the PPC in monkeys performing a spatial version of a match-to-sample task. The task required them to locate salient stimuli in multiple-stimulus displays and release a lever after a subsequent stimulus appeared at the same location. Neurons responded preferentially to the appearance of salient stimuli inside their receptive fields. The presence of multiple stimuli did not affect appreciably the spatial tuning of responses in the majority of neurons or the population code for the location of the salient stimulus. Responses to salient stimuli could be distinguished from background stimuli approximately 100 ms after the onset of the cue. These results suggest that area 7a neurons represent the location of the stimulus attracting the animal's attention and can provide the spatial information required for directing attention to a salient stimulus in a complex scene.     

Intermodal selective attention in monkeys. I: distribution and timing of effects across visual areas

This study quantified the magnitude and timing of selective attention effects across areas of the macaque visual system, including the lateral geniculate nucleus (LGN), lower cortical areas V1 and V2, and multiple higher visual areas in the dorsal and ventral processing streams. We used one stimulus configuration and behavioral paradigm, with simultaneous recordings from different areas to allow direct comparison of the distribution and timing of attention effects across the system. Streams of interdigitated auditory and visual stimuli were presented at a high rate with an irregular interstimulus interval (mean of 4/s). Attention to visual stimuli was manipulated by requiring subjects to make discriminative behavioral responses to stimuli in one sensory modality, ignoring all stimuli in the other. The attended modality was alternated across trial blocks, and difficulty of discrimination was equated across modalities. Stimulus presentation was gated, so that no stimuli were presented unless the subject gazed at the center of the visual stimulus display. Visual stimuli were diffuse light flashes differing in intensity or color and subtending 12 degrees centered at the point of gaze. Laminar event-related potential (ERP) and current source density (CSD) response profiles were sampled during multiple paired penetrations in multiple visual areas with linear array multicontact electrodes. Attention effects were assessed by comparing responses to specific visual stimuli when attended versus when visual stimuli were looked at the same way, but ignored. Effects were quantified by computing a modulation index (MI), a ratio of the differential CSD response produced by attention to the sum responses to attended and ignored visual stimuli. The average MI increased up levels of the lower visual pathways from none in the LGN to 0.0278 in V1 to 0.101 in V2 to 0.170 in V4. Above the V2 level, attention effects were larger in ventral stream areas (MI = 0. 152) than in dorsal stream areas (MI = 0.052). Although onset latencies were shortest in dorsal stream areas, attentional modulation of the early response was small relative to the stimulus-evoked response. Higher ventral stream areas showed substantial attention effects at the earliest poststimulus time points, followed by the lower visual areas V2 and V1. In all areas, attentional modulation lagged the onset of the stimulus-evoked response, and attention effects grew over the time course of the neuronal response. The most powerful, consistent, and earliest attention effects were those found to occur in area V4, during the 100-300 ms poststimulus interval. Smaller effects occurred in V2 over the same interval, and the bulk of attention effects in V1 were later. In the accompanying paper, we describe the physiology of attention effects in V1, V2 and V4.     

Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkey

Perception of two- and three-dimensional optic flow critically depends upon extrastriate cortices that are part of the 'dorsal stream' for visual processing. Neurons in area 7a, a sub-region of the posterior parietal cortex, have a dual sensitivity to visual input and to eye position. The sensitivity and selectivity of area 7a neurons to three sensory cues - optic flow, retinotopic stimulus position and eye position - were studied. The visual response to optic flow was modulated by the retinotopic stimulus position and by the eye position in the orbit. The position dependence of the retinal and eye position modulation (i.e. gain field) were quantified by a quadratic regression model that allowed for linear or peaked receptive fields. A local maximum (or minimum) in both the retinotopic fields and the gain fields was observed, suggesting that these sensory qualities are not necessarily linearly represented in area 7a. Neurons were also found that simply encoded the eye position in the absence of optic flow. The spatial tuning for the eye position signals upon stationary stimuli and optic flow was not the same, suggesting multiple anatomical sources of the signals. These neurons can provide a substrate for spatial representation while primates move in the environment.      

Dorsal posterior parietal rTMS affects voluntary orienting of visuospatial attention

Patients with lesions in posterior parietal cortex (PPC) are relatively unimpaired in voluntarily directing visual attention to different spatial locations, while many neuroimaging studies in healthy subjects suggest dorsal PPC involvement in this function. We used an offline repetitive transcranial magnetic stimulation (rTMS) protocol to study this issue further. Ten healthy participants performed a cue-target paradigm. Cues prompted covert orienting of spatial attention under voluntary control to either a left or right visual field position. Targets were flashed subsequently at the cued or uncued location, or bilaterally. Following rTMS over right dorsal PPC, (i) the benefit for target detection at cued versus uncued positions was preserved irrespective of cueing direction (left- or rightward), but (ii) leftward cueing was associated with a global impairment in target detection, at all target locations. This reveals that leftward orienting was still possible after right dorsal PPC stimulation, albeit at an increased overall cost for target detection. In addition, rTMS (iii) impaired left, but (iv) enhanced right target detection after rightward cueing. The finding of a global drop in target detection during leftward orienting with a spared, relative detection benefit at the cued (left) location (i-ii) suggests that right dorsal PPC plays a subsidiary rather than pivotal role in voluntary spatial orienting. This finding reconciles seemingly conflicting results from patients and neuroimaging studies. The finding of attentional inhibition and enhancement occurring contra- and ipsilaterally to the stimulation site (iii-iv) supports the view that spatial attention bias can be selectively modulated through rTMS, which has proven useful to transiently reduce visual hemispatial neglect.     

Human ventral parietal cortex plays a functional role on visuospatial attention and primary consciousness. A repetitive transcranial magnetic stimulation study

In this paper, we used repetitive transcranial magnetic stimulation (rTMS) in 18 normal subjects to investigate whether the ventral posterior parietal cortex (PPC) plays a causal role on visuospatial attention and primary consciousness and whether these 2 functions are linearly correlated with each other. Two distinct experimental conditions involved a similar visual stimuli recognition paradigm. In "Consciousness" experiment, number of consciously perceived visual stimuli was lower by about 10% after rTMS (300 ms, 20 Hz, motor threshold intensity) on left or right PPC than after sham (pseudo) rTMS. In "Attentional" Posner's experiment, these stimuli were always consciously perceived. Compared with sham condition, parietal rTMS slowed of about 25 ms reaction time to go stimuli, thus disclosing effects on endogenous covert spatial attention. No linear correlation was observed between the rTMS-induced impairment on attention and conscious perception. Results suggest that PPC plays a slight but significant causal role in both visuospatial attention and primary consciousness. Furthermore, these high-level cognitive functions, as modulated by parietal rTMS, do not seem to share either linear or simple relationships.     

Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention

The control of visuospatial attention entails multiple processes, including both voluntary (endogenous) factors and stimulus-driven (exogenous) factors. Exogenous processes can be triggered by visual targets presented at a previously unattended location, thus capturing attention in a stimulus-driven manner. However, little is known about the relative role of stimulus salience and behavioral relevance for this type of spatial reorienting. Here, we directly assessed how salience and relevance affect activation of the frontoparietal attentional system, using either low-salience but task-relevant target stimuli or salient but task-irrelevant flickering checkerboards. We compared event-related functional magnetic resonance imaging responses for stimuli presented at the unattended versus attended side (invalid minus valid trials), separately for the 2 categories of visual stimuli. We found that task-relevant invalid targets activated the frontoparietal attentional network, demonstrating that this system engages when target stimuli are presented at an unattended location, even when these have a low perceptual salience. Conversely, the presentation of high-salience checkerboards in one hemifield while endogenous attention was engaged elsewhere did not activate the attentional network. These findings indicate that task relevance is critical for stimulus-driven engagement of the attentional network when attentional resources are endogenously allocated somewhere else.     

Impaired filtering of distracter stimuli by TE neurons following V4 and TEO lesions in macaques

Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effects of other nearby stimuli. Correspondingly, physiological studies indicate that attention serves to filter distracting stimuli from receptive fields (RFs) in several extrastriate areas. Moreover, a recent study demonstrated that lesions of extrastriate areas V4 and TEO produce impairments in attentional filtering. A critical remaining question concerns why lesions of ventral stream areas cause attentional filtering impairments. To address this question, we tested the effects of restricted area V4 and TEO lesions on both behavioral performance and the responses of downstream neurons in area TE. The lesions impaired behavioral discrimination thresholds and altered neuronal selectivity for target stimuli in the presence of distracters. With attention to the target, but in the absence of V4 and/or TEO inputs, TE neurons responded as though attentional inputs could no longer be used to filter distracters from their RFs. This presumably occurred because top-down attentional signals were no longer able to filter distracters from the RFs of the cells that provide TE with major input. Consistent with this interpretation, increasing the spatial separation between targets and distracters, such that they no longer fell within a typical V4 RF dimension, restored both behavioral performance and neuronal selectivity in the portion of TE RFs affected by the V4 lesion.     

Neural correlates of spatial judgement during object construction in parietal cortex

We recorded the activity of parietal area 7a neurons in monkeys performing an object construction task. In each trial, a model object consisting of a variable arrangement of squares was presented, followed after a delay by a copy of the model object that was missing a single square. Monkeys replaced the missing square to reconstruct the model configuration. Activity of many 7a neurons varied systematically with the position of the missing square and predicted where monkeys were going to add parts to the object they were building. The location of the missing square was a computed spatial datum important to object construction which did not correlate with the retinal location of a visual stimulus or the direction of the required motor response. The population of cells coding this coordinate was generally inactive when the same spatial locations were made relevant by visual targets to which monkeys either planned saccades or directed attention in other behavioral contexts. The data suggest that some parietal neurons participate in neural representations of space that reflect spatial cognitive as opposed to sensorimotor processing, coding the results of spatial computations performed on visual stimuli to meet cognitive objectives.     

Neural responses during interception of real and apparent circularly moving stimuli in motor cortex and area 7a

We recorded the neuronal activity in the arm area of the motor cortex and parietal area 7a of two monkeys during interception of stimuli moving in real and apparent motion. The stimulus moved along a circular path with one of five speeds (180-540 degrees/s), and was intercepted at 6 o'clock by exerting a force pulse on a semi-isometric joystick which controlled a cursor on the screen. The real stimuli were shown in adjacent positions every 16 ms, whereas in the apparent motion situation five stimuli were flashed successively at the vertices of a regular pentagon. The results showed, first, that a group of neurons in both areas above responded not only during the interception but also during a NOGO task in which the same stimuli were presented in the absence of a motor response. This finding suggests these areas are involved in both the processing of the stimulus as well as in the preparation and production of the interception movement. In addition, a group of motor cortical cells responded during the interception task but not during a center --> out task, in which the monkeys produced similar force pulses towards eight stationary targets. This group of cells may be engaged in sensorimotor transformations more specific to the interception of real and apparent moving stimuli. Finally, a multiple regression analysis revealed that the time-varying neuronal activity in area 7a and motor cortex was related to various aspects of stimulus motion and hand force in both the real and apparent motion conditions, with stimulus-related activity prevailing in area 7a and hand-related activity prevailing in motor cortex. In addition, the neural activity was selectively associated with the stimulus angle during real motion, whereas it was tightly correlated to the time-to-contact in the apparent motion condition, particularly in the motor cortex. Overall, these observations indicate that neurons in motor cortex and area 7a are processing different parameters of the stimulus depending on the kind of stimulus motion, and that this information is used in a predictive fashion in motor cortex to trigger the interception movement.     

Spatiotemporal effects of microsaccades on population activity in the visual cortex of monkeys during fixation

During visual fixation, the eyes make fast involuntary miniature movements known as microsaccades (MSs). When MSs are executed they displace the visual image over the retina and can generate neural modulation along the visual pathway. However, the effects of MSs on neural activity have substantial variability and are not fully understood. By utilizing voltage-sensitive dye imaging, we imaged the spatiotemporal patterns induced by MSs in V1 and V2 areas of behaving monkeys while they were fixating and presented with visual stimuli. We then investigated the neuronal modulation dynamics, induced by MSs, under different visual stimulation. MSs induced monophasic or biphasic neural responses depending on stimulus size. These neural responses were accompanied by different spatiotemporal patterns of synchronization. Finally, we show that a local patch of population response evoked by a small stimulus was clearly shifted over the V1 retinotopic map after each MS. Our results demonstrate the lack of visual stability in V1 following MSs and help clarify the substantial variability reported for MSs effects on neuronal responses. The observed neural effects suggest that MSs are associated with a continuum of neuronal responses in V1 area reflecting diverse spatiotemporal dynamics.     

Visual quality determines the direction of neural repetition effects

One ubiquitous finding in functional magnetic resonance imaging studies is that repeated stimuli elicit lower responses than novel stimuli. In apparent contradiction, some studies have reported the exact opposite effect--greater responses to repeated than novel stimuli--in many of the same brain regions. Interestingly, these latter enhancement effects are typically obtained when stimuli have been degraded. To explore this observation, the present study examines the degree to which visual quality mediates repetition effects in a stimulus-selective ventral visual area. Subjects were presented with grayscale photographs of scenes that were either near or substantially above visual threshold, as determined by calibrating image contrast to behavioral performance. The presentation of 2 identical high-contrast scenes elicited lower blood oxygen level-dependent (BOLD) responses than the presentation of 2 different high-contrast scenes (repetition attenuation). Conversely, the presentation of 2 identical low-contrast scenes elicited greater BOLD responses than the presentation of 2 different low-contrast scenes (repetition enhancement). Neurophysiological studies suggest that repetition attenuation in ventral visual areas may reflect the reactivation of perceptual representations that have become sparse and selective as a result of prior experience, whereas repetition enhancement may reflect spared access to existing representations by severely degraded input.     

Cortical neuronal responses to optic flow are shaped by visual strategies for steering

We hypothesized that neuronal responses to virtual self-movement would be enhanced during steering tasks. We recorded the activity of medial superior temporal (MSTd) neurons in monkeys trained to steer a straight-ahead course, using optic flow. We found smaller optic flow responses during active steering than during the passive viewing of the same stimuli. Behavioral analysis showed that the monkeys had learned to steer using local motion cues. Retraining the monkeys to use the global pattern of optic flow reversed the effects of the active-steering task: active steering then evoked larger responses than passive viewing. We then compared the responses of neurons during active steering by local motion and by global patterns: Local motion trials promoted the use of local dot movement near the center of the stimulus by occluding the peripheral visual field midway through the trial. Global pattern trials promoted the use of radial pattern movement by occluding the central visual field midway through the trial. In this study, identical full-field optic-flow stimuli evoked larger responses in global-pattern trials than in local motion trials. We conclude that the selection of specific visual cues reflects strategies for active steering and alters MSTd neuronal responses to optic flow.     

A pure salience response in posterior parietal cortex

When exploring a visual scene, some objects perceptually popout because of a difference of color, shape, or size. This bottom-up information is an important part of many models describing the allocation of visual attention. It has been hypothesized that the lateral intraparietal area (LIP) acts as a "priority map," integrating bottom-up and top-down information to guide the allocation of attention. Despite a large literature describing top-down influences in LIP, the presence of a pure salience response to a salient stimulus defined by its static features alone has not been reported. We compared LIP responses with colored salient stimuli and distractors in a passive fixation task. Many LIP neurons responded preferentially to 1 of the 2 colored stimuli, yet the mean responses to the salient stimuli were significantly higher than to distractors, independent of the features of the stimuli. These enhanced responses were significant within 75 ms, and the mean responses to salient and distractor stimuli were tightly correlated, suggesting a simple gain control. We propose that a pure salience signal rapidly appears in LIP by collating salience signals from earlier visual areas. This contributes to the creation of a priority map, which is used to guide attention and saccades.     

Persistent discharges in the prefrontal cortex of monkeys naive to working memory tasks

Neurons in the prefrontal cortex and a network of interconnected brain areas discharge in a persistent fashion after the offset of sensory stimulation. Such persistent discharges are thought to constitute a neuronal correlate of working memory. The information content of neuronal discharges and its anatomical localization across the surface of the prefrontal cortex has been a matter of debate. Discrepant results by different laboratories may be due to the effects of different training regiments and tasks used in memory tasks. In order to address how training in a memory task alters neuronal responses, we performed recordings in monkeys that were never trained in memory tasks, but passively viewed visual stimuli. We have found that a population of prefrontal neurons responded to visual stimuli and also exhibited significantly elevated responses during "delay" intervals of the task. For a population of these neurons, persistent discharges were selective for the location and feature of the preceding stimulus. These discharges were typically disrupted by the appearance of a subsequent stimulus. Our results suggest that some prefrontal neurons represent the location and identity of visual stimuli in a persistent fashion, even when the latter are not behaviorally important or required to be kept in memory.     

Synchrony dynamics in monkey V1 predict success in visual detection

Behavioral measures such as expectancy and attention have been associated with the strength of synchronous neural activity. On this basis, it is hypothesized that synchronous activity affects our ability to detect and recognize visual objects. To investigate the role of synchronous activity in visual perception, we studied the magnitude and precision of correlated activity, before and after stimulus presentation within the visual cortex (V1), in relation to a monkey's performance in a figure-ground discrimination task. We show that during the period of stimulus presentation a transition in synchronized activity occurs that is characterized by a reduction of the correlation peak height and width. Before stimulus onset, broad peak correlations are observed that change towards thin peak correlations after stimulus onset, due to a specific decrease of low-frequency components. The magnitude of the transition in correlated activity is larger, i.e. a stronger desynchronization occurs, when the animal perceives the stimulus correctly than when the animal fails to detect the stimulus. These results therefore show that a transition in synchronous firing is important for the detection of sensory stimuli. We hypothesize that the transition in synchrony reflects a change from loose and global neuronal interactions towards a finer temporal and spatial scale of neuronal interactions, and that such a change in neuronal interactions is required for figure-ground discrimination.     

Inferior Temporal Mechanisms for Invariant Object Recognition

The specific size and retinal location of an object are readilyperceived, yet recognition of an object's identity is hardlyaffected by transformations of its size or location, To explorehow such stimulus transformations are treated by known mechanismsfor visual short-term memory in inferior temporal (IT) cortex,IT cells were recorded in monkeys performing a delayed matching-to-sampletask. The stimuli were pictures of complex objects, and themonkeys ignored differences in size and retinal location whenmatching the test items to the sample held in memory. The sensoryinformation communicated by cells was assessed in their responsesto the sample stimuli, and mnemonic information was assessedin their responses to the test stimuli. In the sensory domain,the ordering of relative stimulus preferences for nearly allcells was invariant over changes in size or location; however,some cells nonetheless preferred stimuli of a given size orlocation. In the mnemonic domain, the responses of many cellswere modulated according to whether the test stimulus matchedthe sample held in memory, and these memory effects were invariantover the relative sizes and locations of the stimuli. Thus,IT neuronal populations may mediate not only the recognitionand memory of object identity, which are invariant over sizeand location, but also the perception of the transformationsthemselves.     

Effect of systemic morphine on the responses of convergent neurons to noxious heat stimuli applied over graded surface areas

BACKGROUND: Stimulus intensity is a major determinant of the antinociceptive activity of opiates. This study focused on the influence of the spatial characteristics of nociceptive stimuli, on opiate-induced depressions of nociceptive transmission at the level of the spinal cord. METHODS: Anesthetized rats were prepared to allow extracellular recordings to be made from convergent neurons in the lumbar dorsal horn. The effects of systemic morphine (1 and 10 mg/kg) were compared with those of saline for thermal stimuli of constant intensity, applied to the area of skin surrounding the excitatory receptive field (1.9 cm2) or to a much larger adjacent area (18 cm2). RESULTS: The responses (mean +/- SD) elicited by the 1.9-cm2 stimulus were not modified by 1 mg/kg intravenous morphine, although they were decreased by the 10-mg/kg dose (to 11+/-4% of control values compared with saline; P < 0.05). In contrast, when the 18-cm2 stimulus was applied, 1 mg/kg intravenous morphine produced a paradoxical facilitation of the neuronal responses (159+/-36% of control values; P < 0.05) and 10 mg/kg intravenous morphine resulted in a weaker depression of the responses (to 42+/-24% of control values; P < 0.05) than was observed with the smaller stimulus. CONCLUSIONS: Doses of systemic morphine in the analgesic range for rats had dual effects on nociceptive transmission at the level of the spinal cord, depending on the surface area that was stimulated. Such effects are difficult to explain in terms of accepted pharmacodynamic concepts and may reflect an opioid-induced depression of descending inhibitory influences triggered by spatial summation.     

Source analysis of event-related cortical activity during visuo-spatial attention

Recordings of event-related potentials (ERPs) were combined with structural and functional magnetic resonance imaging (fMRI) to study the spatio-temporal patterns of cortical activity that underlie visual-spatial attention. Small checkerboard stimuli were flashed in random order to the four quadrants of the visual field at a rapid rate while subjects attended to stimuli in one quadrant at a time. Attended stimuli elicited enhanced ERP components in the latency range 80-200 ms that were co-localized with fMRI activations in multiple extrastriate cortical regions. The earliest ERP component (C1 at 50-90 ms) was unaffected by attention and was localized by dipole modeling to calcarine cortex. A longer latency deflection in the 150-225 ms range that was accounted for by this same calcarine source, however, did show consistent modulation with attention. This late attention effect, like the C1, inverted in polarity for upper versus lower field stimuli, consistent with a neural generator in primary visual cortex (area V1). These results provide support to current hypotheses that spatial attention in humans is associated with delayed feedback to area V1 from higher extrastriate areas that may have the function of improving the salience of stimuli at attended locations.     

The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts

How does the human brain integrate information from multiple domains to guide spatial attention according to motivational needs? To address this question, we measured hemodynamic responses to central cues predicting locations of peripheral attentional targets (food or tool images) in a novel covert spatial attention paradigm. The motivational relevance of food-related attentional targets was experimentally manipulated via hunger and satiety. Amygdala, posterior cingulate, locus coeruleus, and substantia nigra showed selective sensitivity to food-related cues when hungry but not when satiated, an effect that did not generalize to tools. Posterior parietal cortex (PPC), including intraparietal sulcus, posterior cingulate, and the orbitofrontal cortex displayed correlations with the speed of attentional shifts that were sensitive not just to motivational state but also to the motivational value of the target. Stronger functional coupling between PPC and posterior cingulate occurred during attentional biasing toward motivationally relevant food targets. These results reveal conjoint limbic and monoaminergic encoding of motivational salience in spatial attention. They emphasize the interactive role of posterior parietal and cingulate cortices in integrating motivational information with spatial attention, a process that is critical for selective allocation of attentional resources in an environment where target position and relevance can change rapidly.     

Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex

When multiple objects are present in a visual scene, they compete for cortical processing in the visual system; selective attention biases this competition so that representations of behaviorally relevant objects enter awareness and irrelevant objects do not. Deployments of selective attention can be voluntary (e.g., shift or attention to a target's expected spatial location) or stimulus driven (e.g., capture of attention by a target-defining feature such as color). Here we use functional magnetic resonance imaging to show that both of these factors induce spatially selective attentional modulations within regions of human occipital, parietal, and frontal cortex. In addition, the voluntary attentional modulations are temporally sustained, indicating that activity in these regions dynamically tracks the locus of attention. These data show that a convolution of factors, including prior knowledge of location and target-defining features, determines the relative competitive advantage of visual stimuli within multiple stages of the visual system.