Papers by Robert Desimone

Neuron, 2016
The ventro-lateral pulvinar is reciprocally connected with the visual areas of the ventral stream... more The ventro-lateral pulvinar is reciprocally connected with the visual areas of the ventral stream important for object recognition. To understand the mechanisms of attentive stimulus processing in this pulvinar-cortex loop, we investigated the interactions between the pulvinar, area V4, and IT cortex in a spatial attention task. Sensory processing and the influence of attention in the pulvinar appeared to reflect its cortical inputs. However, pulvinar deactivation led to a reduction of attentional effects on firing rates and gamma synchrony in V4, a reduction of sensory-evoked responses and overall gamma coherence within V4, and severe behavioral deficits in the affected portion of the visual field. Conversely, pulvinar deactivation caused an increase in low frequency cortical oscillations, often associated with inattention or sleep. Thus, cortical interactions with the ventro-lateral pulvinar are necessary for normal attention and sensory processing, and for maintaining the cortex in an active state.
Progress in Brain Research, 2009
In a crowded visual scene, we typically employ attention to select stimuli that are behaviorally ... more In a crowded visual scene, we typically employ attention to select stimuli that are behaviorally relevant. Two likely cortical sources of top-down attentional feedback to cortical visual areas are the prefrontal (PFC) and posterior parietal (PPC) cortices. Recent neurophysiological studies show that areas in PFC and PPC process signals about the locus of attention earlier than in extrastriate visual areas and are therefore likely to mediate attentional selection. Moreover, attentional selection appears to be mediated in part by neural synchrony between neurons in PFC/PPC and early visual areas, with phase relationships that seem optimal for increasing the impact of the top-down inputs to the visual cortex.

Neuron, 2011
When we search for a target in a crowded visual scene, we often use the distinguishing features o... more When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.

Neuron, 2012
Shifts of gaze and shifts of attention are closely linked and it is debated whether they result f... more Shifts of gaze and shifts of attention are closely linked and it is debated whether they result from the same neural mechanisms. Both processes involve the frontal eye fields (FEF), an area which is also a source of top-down feedback to area V4 during covert attention. To test the relative contributions of oculomotor and attention-related FEF signals to such feedback, we recorded simultaneously from both areas in a covert attention task and in a saccade task. In the attention task, only visual and visuomovement FEF neurons showed enhanced responses, whereas movement cells were unchanged. Importantly, visual, but not movement or visuomovement cells, showed enhanced gamma frequency synchronization with activity in V4 during attention. Within FEF, beta synchronization was increased for movement cells during attention but was suppressed in the saccade task. These findings support the idea that the attentional modulation of visual processing is not mediated by movement neurons.

Responses of cells in the superior colliculus during performance of a spatial attention task in the macaque
Revista brasileira de biologia, 1996
Previous studies have reported that superficial layer cells in the superior colliculus (SC) give ... more Previous studies have reported that superficial layer cells in the superior colliculus (SC) give an enhanced response to a stimulus when it is the target for an eye movement. However, in a peripheral detection paradigm, no such enhancement was found when a stimulus was attended, in the absence of an eye movement. Inasmuch as behavioral studies have found attention deficits in the absence of eye movements following SC lesions or deactivation, we investigated this issue in a paradigm that is very sensitive to effects of attention. In a matching-to-sample paradigm, a sample stimulus was presented at one location followed by a brief test stimulus at that (relevant) location and a distracter at another (irrelevant) location. While maintaining fixation, the monkey indicated whether the sample and the test stimulus matched, ignoring the distracter. The relevant and irrelevant locations were switched from trial to trial. SC cells in the superficial layers tended to give enhanced responses w...

Neuron, 2015
In cluttered scenes, we can use feature-based attention to quickly locate a target object. To und... more In cluttered scenes, we can use feature-based attention to quickly locate a target object. To understand how feature attention is used to find and select objects for action, we focused on the ventral pre-arcuate (VPA) region of prefrontal cortex. In a visual search task, VPA cells responded selectively to search cues, maintained their feature selectivity throughout the delay and subsequent saccades, and discriminated the search target in their receptive fields with a timecourse earlier than in FEF or IT cortex. Inactivation of VPA impaired the animals' ability to find targets, and simultaneous recordings in FEF revealed that the effects of feature attention were eliminated while leaving the effects of spatial attention in FEF intact. Altogether, the results suggest that VPA neurons compute the locations of objects with the features sought and send this information to FEF to guide eye movements to those relevant stimuli.

Proceedings of the National Academy of Sciences, 2010
The visual processing of behaviorally relevant stimuli is enhanced through top-down attentional f... more The visual processing of behaviorally relevant stimuli is enhanced through top-down attentional feedback. One possibility is that feedback targets early visual areas first and the attentional enhancement builds up at progressively later stages of the visual hierarchy. An alternative possibility is that the feedback targets the higher-order areas first and the attentional effects are communicated "backward" to early visual areas. Here, we compared the magnitude and latency of attentional enhancement of firing rates in V1, V2, and V4 in the same animals performing the same task. We found a reverse order of attentional effects, such that attentional enhancement was larger and earlier in V4 and smaller and later in V1, with intermediate results in V2. These results suggest that attentional mechanisms operate via feedback from higher-order areas to lower-order ones.

Neuron, 1999
scene. When multiple stimuli are presented simultaneously in a neuron's receptive field (RF) in a... more scene. When multiple stimuli are presented simultaneously in a neuron's receptive field (RF) in areas V2, V4, or the inferior temporal cortex, and the animal directs its attention to one of them, the neuron's response is determined primarily by the attended stimulus (Moran . Recent work suggests that this atten-Bethesda, Maryland 20892 tional selection operates by biasing an underlying competitive interaction among multiple stimuli in the visual field. The most direct evidence for such competition Summary is the fact that the response to an otherwise effective stimulus presented within a neuron's RF is reduced When subjects direct attention to a particular location when a second stimulus is presented simultaneously at in a visual scene, responses in the visual cortex to a different location within the same RF (Sato, 1989; Miller stimuli presented at that location are enhanced, and et al., 1993; Reynolds et al., 1999). Attending to the the suppressive influences of nearby distractors are effective stimulus eliminates the suppressive influence reduced. What is the top-down signal that modulates of the second stimulus (Moran and Desimone, 1985; the response to an attended versus an unattended Reynolds et al., 1999). Thus, spatially directed attention stimulus? Here, we demonstrate increased activity reoperates by counteracting the suppressive influences lated to attention in the absence of visual stimulation of nearby stimuli, thereby enhancing information proin extrastriate cortex when subjects covertly directed cessing at the attended location. Additional evidence attention to a peripheral location expecting the onset for the top-down bias favoring an attended stimulus of visual stimuli. Frontal and parietal areas showed a location is the finding that stimulus-evoked responses stronger signal increase during this expectation than to a RF stimulus are sometimes higher in areas V2 and did visual areas. The increased activity in visual cortex V4 when the stimulus is attended (Spitzer et al., 1988; in the absence of visual stimulation may reflect a top-Motter , and, strikingly, the spontaneous (basedown bias of neural signals in favor of the attended line) firing rates are 30%-40% higher in these same location, which derives from a fronto-parietal network.

Responses of neurons in inferior temporal cortex during memory-guided visual search
Journal of neurophysiology, 1998
Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophys... more Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophysiol. 80: 2918-2940, 1998. A typical scene will contain many different objects, few of which are relevant to behavior at any given moment. Thus attentional mechanisms are needed to select relevant objects for visual processing and control over behavior. We examined this role of attention in the inferior temporal cortex of macaque monkeys, using a visual search paradigm. While the monkey maintained fixation, a cue stimulus was presented at the center of gaze, followed by a blank delay period. After the delay, an array of two to five choice stimuli was presented extrafoveally, and the monkey was rewarded for detecting a target stimulus matching the cue. The behavioral response was a saccadic eye movement to the target in one version of the task and a lever release in another. The array was composed of one "good" stimulus (effective in driving the cell when presented alone) and one...

Journal of neurophysiology, 1986
Although the tectofugal system projects to the primate cerebral cortex by way of the pulvinar, pr... more Although the tectofugal system projects to the primate cerebral cortex by way of the pulvinar, previous studies have failed to find any physiological evidence that the superior colliculus influences visual activity in the cortex. We studied the relative contributions of the tectofugal and geniculostriate systems to the visual properties of neurons in the superior temporal polysensory area (STP) by comparing the effects of unilateral removal of striate cortex, the superior colliculus, or of both structures. In the intact monkey, STP neurons have large, bilateral receptive fields. Complete unilateral removal of striate cortex did not eliminate visual responses of STP neurons in the contralateral visual hemifield; rather, nearly half the cells still responded to visual stimuli in the hemifield contralateral to the lesion. Thus the visual properties of STP neurons are not completely dependent on the geniculostriate system. Unilateral striate lesions did affect the response properties of...

Nature neuroscience, 2014
It is widely held that the frontal eye field (FEF) in prefrontal cortex (PFC) modulates processin... more It is widely held that the frontal eye field (FEF) in prefrontal cortex (PFC) modulates processing in visual cortex with attention, although the evidence that it is necessary is equivocal. To help identify critical sources of attentional feedback to area V4, we surgically removed the entire lateral PFC, including the FEF, in one hemisphere and transected the corpus callosum and anterior commissure in two macaques. This deprived V4 of PFC input in one hemisphere while keeping the other hemisphere intact. In the absence of PFC, attentional effects on neuronal responses and synchrony in V4 were substantially reduced and the remaining effects of attention were delayed in time, indicating a critical role for PFC. Conversely, distracters captured attention and influenced V4 responses. However, because the effects of attention in V4 were not eliminated by PFC lesions, other sources of top-down attentional control signals to visual cortex must exist outside of PFC.

Learning increases stimulus salience in anterior inferior temporal cortex of the macaque
Journal of neurophysiology, 2001
With experience, an object can become behaviorally relevant and thereby quickly attract our inter... more With experience, an object can become behaviorally relevant and thereby quickly attract our interest when presented in a visual scene. A likely site of these learning effects is anterior inferior temporal (aIT) cortex, where neurons are thought to participate in the filtering of irrelevant information out of complex visual displays. We trained monkeys to saccade consistently to one of two pictures in an array, in return for a reward. The array was constructed by pairing two stimuli, one of which elicited a good response from the cell when presented alone ("good" stimulus) and the other of which elicited a poor response ("poor" stimulus). The activity of aIT cells was recorded while monkeys learned to saccade to either the good or poor stimulus in the array. We found that neuronal responses to the array were greater (before the saccade occurred) when training reinforced a saccade to the good stimulus than when training reinforced a saccade to the poor stimulus. Th...
Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI
Science (New York, N.Y.), Jan 2, 1998
A typical scene contains many different objects, but the capacity of the visual system to process... more A typical scene contains many different objects, but the capacity of the visual system to process multiple stimuli at a given time is limited. Thus, attentional mechanisms are required to select relevant objects from among the many objects competing for visual processing. Evidence from functional magnetic resonance imaging (MRI) in humans showed that when multiple stimuli are present simultaneously in the visual field, their cortical representations within the object recognition pathway interact in a competitive, suppressive fashion. Directing attention to one of the stimuli counteracts the suppressive influence of nearby stimuli. This mechanism may serve to filter out irrelevant information in cluttered visual scenes.

Journal of neurophysiology, 1997
Many neurons in extrastriate visual cortex have large receptive fields, and this may lead to sign... more Many neurons in extrastriate visual cortex have large receptive fields, and this may lead to significant computational problems whenever multiple stimuli fall within a single field. Previous studies have suggested that when multiple stimuli fall within a cell's receptive field, they compete for the cell's response in a manner that can be biased in favor of attended stimuli. In the present study we examined this role of attention in areas V1, V2, and V4 of macaque monkeys with the use of a behavioral paradigm in which attention was directed to one of two stimulus locations. When two stimuli were presented simultaneously inside the cell's receptive field (which could be accomplished only in areas V2 and V4), we found that the cell's response was strongly influenced by which of the two stimuli was attended. The size of this attention effect was reduced when the attended and ignored stimuli were presented sequentially rather than simultaneously. In addition, the effects ...
Journal of neurophysiology, 1981

The Journal of neuroscience : the official journal of the Society for Neuroscience, 1991
It has been proposed that visual information in the extrastriate cortex is conveyed along 2 major... more It has been proposed that visual information in the extrastriate cortex is conveyed along 2 major processing pathways, a "dorsal" pathway directed to the posterior parietal cortex, underlying spatial vision, and a "ventral" pathway directed to the inferior temporal cortex, underlying object vision. To determine the relative distributions of cells projecting to the 2 pathways, we injected the posterior parietal and inferior temporal cortex with different fluorescent tracers in 5 rhesus monkeys. The parietal injections included the ventral intraparietal (VIP) and lateral intraparietal (LIP) areas, and the temporal injections included the lateral portions of cytoarchitectonic areas TE and TEO. There was a remarkable segregation of cells projecting to the 2 systems. Inputs to the parietal cortex tended to arise either from areas that have been implicated in spatial or motion analysis or from peripheral field representations in the prestriate cortex. By contrast, inpu...
Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effec... more Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effects of other nearby stimuli. Corre- spondingly, 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

Effect of distracting faces on visual selective attention in the monkey
Proceedings of the National Academy of Sciences of the United States of America, Jan 16, 2014
In primates, visual stimuli with social and emotional content tend to attract attention. Attentio... more In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade...

Custom-fit radiolucent cranial implants for neurophysiological recording and stimulation
Journal of neuroscience methods, Jan 15, 2015
Recording and manipulating neural activity in awake behaving animal models requires long-term imp... more Recording and manipulating neural activity in awake behaving animal models requires long-term implantation of cranial implants that must address a variety of design considerations, which include preventing infection, minimizing tissue damage, mechanical strength of the implant, and MRI compatibility. Here we address these issues by designing legless, custom-fit cranial implants using structural MRI-based reconstruction of the skull and that are made from carbon-reinforced PEEK. We report several novel custom-fit radiolucent implant designs, which include a legless recording chamber, a legless stimulation chamber, a multi-channel microdrive and a head post. The fit to the skull was excellent in all cases, with no visible gaps between the base of the implants and the skull. The wound margin was minimal in size and showed no sign of infection or skin recession. Cranial implants used for neurophysiological investigation in awake behaving animals often employ methyl methacrylate (MMA) to...
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Papers by Robert Desimone