Attention In Monkeys Research Articles

Brain regions modulated during covert visual attention in the macaque

Neurophysiological studies of covert visual attention in monkeys have emphasized the modulation of sensory neural responses in the visual cortex. At the same time, electrophysiological correlates of attention have been reported in other cortical and subcortical structures, and recent fMRI studies have identified regions across the brain modulated by attention. Here we used fMRI in two monkeys performing covert attention tasks to reproduce and extend these findings in order to help establish a more complete list of brain structures involved in the control of attention. As expected from previous studies, we found attention-related modulation in frontal, parietal and visual cortical areas as well as the superior colliculus and pulvinar. We also found significant attention-related modulation in cortical regions not traditionally linked to attention – mid-STS areas (anterior FST and parts of IPa, PGa, TPO), as well as the caudate nucleus. A control experiment using a second-order orientation stimulus showed that the observed modulation in a subset of these mid-STS areas did not depend on visual motion. These results identify the mid-STS areas (anterior FST and parts of IPa, PGa, TPO) and caudate nucleus as potentially important brain regions in the control of covert visual attention in monkeys.

Functional Imaging of Audio-Visual Selective Attention in Monkeys and Humans: How do Lapses in Monkey Performance Affect Cross-Species Correspondences?

The cross-species correspondences and differences in how attention modulates brain responses in humans and animal models are poorly understood. We trained 2 monkeys to perform an audio–visual selective attention task during functional magnetic resonance imaging (fMRI), rewarding them to attend to stimuli in one modality while ignoring those in the other. Monkey fMRI identified regions strongly modulated by auditory or visual attention. Surprisingly, auditory attention-related modulations were much more restricted in monkeys than humans performing the same tasks during fMRI. Further analyses ruled out trivial explanations, suggesting that labile selective-attention performance was associated with inhomogeneous modulations in wide cortical regions in the monkeys. The findings provide initial insights into how audio–visual selective attention modulates the primate brain, identify sources for “lost” attention effects in monkeys, and carry implications for modeling the neurobiology of human cognition with nonhuman animals.

Graded Neuronal Modulations Related to Visual Spatial Attention.

Studies of visual attention in monkeys typically measure neuronal activity when the stimulus event to be detected occurs at a cued location versus when it occurs at an uncued location. But this approach does not address how neuronal activity changes relative to conditions where attention is unconstrained by cueing. Human psychophysical studies have used neutral cueing conditions and found that neutrally cued behavioral performance is generally intermediate to that of cued and uncued conditions (Posner et al., 1978; Mangun and Hillyard, 1990; Montagna et al., 2009). To determine whether the neuronal correlates of visual attention during neutral cueing are similarly intermediate, we trained macaque monkeys to detect changes in stimulus orientation that were more likely to occur at one location (cued) than another (uncued), or were equally likely to occur at either stimulus location (neutral). Consistent with human studies, performance was best when the location was cued, intermediate when both locations were neutrally cued, and worst when the location was uncued. Neuronal modulations in visual area V4 were also graded as a function of cue validity and behavioral performance. By recording from both hemispheres simultaneously, we investigated the possibility of switching attention between stimulus locations during neutral cueing. The results failed to support a unitary "spotlight" of attention. Overall, our findings indicate that attention-related changes in V4 are graded to accommodate task demands. Studies of the neuronal correlates of attention in monkeys typically use visual cues to manipulate where attention is focused ("cued" vs "uncued"). Human psychophysical studies often also include neutrally cued trials to study how attention naturally varies between points of interest. But the neuronal correlates of this neutral condition are unclear. We measured behavioral performance and neuronal activity in cued, uncued, and neutrally cued blocks of trials. Behavioral performance and neuronal responses during neutral cueing were intermediate to those of the cued and uncued conditions. We found no signatures of a single mechanism of attention that switches between stimulus locations. Thus, attention-related changes in neuronal activity are largely hemisphere-specific and graded according to task demands.

Orienting of Attention to Gaze Direction Cues in Rhesus Macaques: Species-Specificity, and Effects of Cue Motion and Reward Predictiveness

Primates live in complex social groups and rely on social cues to direct their attention. For example, primates react faster to an unpredictable stimulus after seeing a conspecific looking in the direction of that stimulus. In the current study we tested the specificity of facial cues (gaze direction) for orienting attention and their interaction with other cues that are known to guide attention. In particular, we tested whether macaque monkeys only respond to gaze cues from conspecifics or if the effect generalizes across species. We found an attentional advantage of conspecific faces over human and cartoon faces. Because gaze cues are often conveyed by gesture, we also explored the effect of image motion (a simulated glance) on the orienting of attention in monkeys. We found that the simulated glance did not significantly enhance the speed of orienting for monkey-face stimuli, but had a significant effect for images of human faces. Finally, because gaze cues presumably guide attention toward relevant or rewarding stimuli, we explored whether orienting of attention was modulated by reward predictiveness. When the cue predicted reward location, face, and non-face cues were effective in speeding responses toward the cued location. This effect was strongest for conspecific faces. In sum, our results suggest that while conspecific gaze cues activate an intrinsic process that reflexively directs spatial attention, its effect is relatively small in comparison to other features including motion and reward predictiveness. It is possible that gaze cues are more important for decision-making and voluntary orienting than for reflexive orienting.

Attention Improves Object Representation in Visual Cortical Field Potentials

Selective attention improves perception and modulates neuronal responses, but how attention-dependent changes of cortical activity improve the processing of attended objects is an open question. Changes in total signal strength or enhancements in signal-to-noise ratio have been proposed as putative mechanisms. However, it is still not clear whether, and to what extent, these processes contribute to the large perceptual improvements. We studied the ability to discriminate states of activity in visual cortex evoked by differently shaped objects depending on selective attention in monkeys. We found that gamma-band activity from V4 and V1 contains a high amount of information about stimulus shape, which increases for V4 recordings considerably with attention in successful trials, but not in case of behavioral errors. This effect resulted from enhanced differences between the stimulus-specific distributions of power spectral amplitudes. It could be explained neither by enhancements of signal-to-noise ratios, nor by changes in total signal power. Instead our results indicate that attention causes underlying cortical network states to become more distinct for different stimuli, providing a new neurophysiological explanation for improvements of behavioral performance by attention. The absence of the enhancement in discriminability in trials with behavioral errors demonstrates the relevance of this novel neural mechanism for perception.

Spatial Attention Does Not Strongly Modulate Neuronal Responses in Early Human Visual Cortex

Attention can dramatically enhance behavioral performance based on a visual stimulus, but the degree to which attention modulates activity in early visual cortex is unclear. Whereas single-unit studies of spatial attention in monkeys have repeatedly revealed relatively modest attentional modulations in V1, human functional magnetic resonance imaging studies demonstrate a large attentional enhancement of the blood oxygen level-dependent (BOLD) signal in V1. To explore this discrepancy, we used intracranial electrodes to directly measure the effect of spatial attention on the responses of neurons near the human occipital pole. We found that spatial attention does not robustly modulate stimulus-driven local field potentials in early human visual cortex, but instead produces modest modulations that are consistent with those seen in monkey neurophysiology experiments. This finding suggests that the neuronal activity that underlies visual attention in humans is similar to that found in other primates and that behavioral state may alter the linear relationship between neuronal activity and BOLD.

Differences of monkey and human overt attention under natural conditions

Rhesus monkeys are widely used as animal models of human attention. Such research rests upon the assumption that similar mechanisms underlie attention in both species. Here, we directly compare the influence of low-level stimulus features on overt attention in monkeys and humans under natural conditions. We recorded eye-movements in humans and rhesus monkeys during free-viewing of natural images. We find that intrinsic low-level features, such luminance-contrast, texture-contrast and saliency—as predicted by a standard model, are elevated at fixation points in the majority of images. These correlative effects are not significantly different between species. However, local image modifications affect both species differently: moderate modifications, which are in the range of natural fluctuations, attract overt attention in monkeys significantly stronger than they do in humans. In addition, humans show a higher inter-individual consistency regarding which locations they fixate than monkeys, in spite of the similarity for intrinsic low-level features. Taken together, these data demonstrate that—under natural conditions—low-level stimulus features affect attention in monkeys and humans differently.

Reflexive Social Attention in Monkeys and Humans

For humans, social cues often guide the focus of attention. Although many nonhuman primates, like humans, live in large, complex social groups, the extent to which human and nonhuman primates share fundamental mechanisms of social attention remains unexplored. Here, we show that, when viewing a rhesus macaque looking in a particular direction, both rhesus macaques and humans reflexively and covertly orient their attention in the same direction. Specifically, when performing a peripheral visual target detection task, viewing a monkey with either its eyes alone or with both its head and eyes averted to one side facilitated the detection of peripheral targets when they randomly appeared on the same side. Moreover, viewing images of a monkey with averted gaze evoked small but systematic shifts in eye position in the direction of gaze in the image. The similar magnitude and temporal dynamics of response facilitation and eye deviation in monkeys and humans suggest shared neural circuitry mediating social attention.

Task relevance enhances early transient and late slow-wave activity of distributed cortical sources.

The primary purpose of these studies was to link together concepts related to attention/working memory and feedforward/feedback activity using MEG response profiles obtained in humans. Similar to recent studies of attention in monkeys, we show early "spike-like" activity (<200 ms poststimulus), most likely reflecting an early transient excitatory response mixed with feedback influences, followed by "slow-wave" activity (>200 ms poststimulus) in MEG cortical response profiles evoked by a visual working memory task. We experimentally dissociated the early transient activity from the later sustained activity (predominantly feedback) by conducting an auditory size classification task. Words, representing common objects, evoked activity in occipital cortex (presumably due to imagery) even though visual stimuli were not present in this task. The initial "spike" was absent from the response profile obtained from occipital cortex, leaving only "slow-wave" activity, thereby allowing us to characterize or profile feedback activity in this situation. Attention or task relevance enhanced the initial "spike" and "slow-wave" activity in visually responsive areas. Prefrontal activity, along the superior frontal sulcus, evoked by the working memory task, was active later in time than initial activity in visual cortex and later than the earliest effect of attention modulation in visual cortex.

Intermodal Selective Attention in Monkeys. II: Physiological Mechanisms of Modulation

Of all areas studied in the accompanying study, attention effects were most consistent and well resolved in V4. In this study, to define some of the anatomical circuits and neural processes underlying the influence of attention, we examined the laminar distribution and physiology of attention effects in V4 and in two lower areas, V1 and V2. Laminar event-related potential (ERP), current source density (CSD) and multiunit activity (MUA) profiles allowed identification of processes occurring in the local ensembles, as well as their sequence and laminar distribution. These methods also permitted us to analyze the brain processes reflected in attention-sensitive components of the surface ERP. As outlined in the previous study, the first robust modulation by attention occurred in V4 during the 100-300 ms poststimulus interval. This is the time frame of the net refractoriness which follows the net local excitatory response to luminance increment. Over this interval, attention reduced CSD amplitudes and increased action potential firing rates, findings consistent with disinhibition as a mechanism for attention in V4. Similar effects were observed during the 100-300 ms time frame in V2. In V4, attention had no effect on the initial excitatory response at the depth of lamina 4, but it did produce large modulations in supragranular and deep laminae, origins of both feedforward and feedback projections. Attentional modulation in V2 was later than in V4 and concentrated in extragranular laminae, with no modulation of the initial layer 4 response. Attentional modulation in V1 was smaller and still later than that in V2 and was focused in the supragranular laminae. In this paradigm, attention did not modulate either the response in lateral geniculate nucleus (LGN) or the initial excitation in lamina 4C of V1. The timing of effects across areas and the laminar distribution of effects within areas indicate that attention effects are mediated by feedback projections. Moreover, our findings suggest that attention may increase the perceptual salience of stimuli by reducing stimulus-evoked refractoriness and/or inhibition in cortical ensembles. Finally, attentional modulation of transmembrane current flow in V4 produced a sustained negative deflection in the laminar ERP profile, that was manifested in the ERP over the occipital surface. This posits a mechanism for the 'selection negativity', a scalp ERP effect noted under similar experimental conditions in human subjects.

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.

Effects of chlorpromazine, secobarbital and sleep deprivation on attention in monkeys.

In order to develop a method for studying sustained attention in the monkey, animals were trained to perform a rapid, serially-presented visual discrimination task. Two versions of the task were developed, one dependent upon shock avoidance, the other on water reward. The effects of varying doses of chlorpromazine (0.075 to 0.6 mg/kg) and of secobarbital (5 to 25 mg/kg) were studied; the shock avoidance task was also used to measure the effects of continuous work-sleep deprivation for periods up to 48 hours.

Modification of Cortically Induced Responses in Brain Stem by Shift of Attention in Monkeys

Modification of Cortically Induced Responses in Brain Stem by Shift of Attention in Monkeys

Modification of Cortically Induced Responses in Brain Stem by Shift of Attention in Monkeys

The long-latency electrical response of the brain stem evoked by stimulation of the cortex of freely moving monkeys is modified by a change of attention. The modification may be either suppression or augmentation, according to the background activity prior to the shift of attention.