Frontal eye field neurons signal changes in decision criteria

Ferrera, Vincent P.; Yanike, Marianna; Cassanello, Carlos

doi:10.1038/nn.2434

Cited by 83 publications

(66 citation statements)

References 26 publications

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“…4B). Unlike the category codes found in previous work (28,29,42), most of our FEF neurons, as well as the population average, increased their firing when a given interval was perceived as lasting longer. If the neurons represented temporal categories, the "long" category vastly outnumbered the "short" category.…”

Section: Discussioncontrasting

confidence: 96%

Neuronal correlates of visual time perception at brief timescales

Mayo

Sommer

2013

Proc. Natl. Acad. Sci. U.S.A.

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Successful interaction with the world depends on accurate perception of the timing of external events. Neurons at early stages of the primate visual system represent time-varying stimuli with high precision. However, it is unknown whether this temporal fidelity is maintained in the prefrontal cortex, where changes in neuronal activity generally correlate with changes in perception. One reason to suspect that it is not maintained is that humans experience surprisingly large fluctuations in the perception of time. To investigate the neuronal correlates of time perception, we recorded from neurons in the prefrontal cortex and midbrain of monkeys performing a temporal-discrimination task. Visual time intervals were presented at a timescale relevant to natural behavior (<500 ms). At this brief timescale, neuronal adaptationtime-dependent changes in the size of successive responsesoccurs. We found that visual activity fluctuated with timing judgments in the prefrontal cortex but not in comparable midbrain areas. Surprisingly, only response strength, not timing, predicted task performance. Intervals perceived as longer were associated with larger visual responses and shorter intervals with smaller responses, matching the dynamics of adaptation. These results suggest that the magnitude of prefrontal activity may be read out to provide temporal information that contributes to judging the passage of time.vision | frontal eye field | superior colliculus | macaque | latency S ystems neuroscience research has focused on the spatial aspects of vision, including form, orientation, and size (1, 2). However, the role of time in vision is no less important. Research on the temporal aspects of primate vision has largely consisted of studies of the temporal dynamics of neural activity in the early stages of visual processing, where neurons are exquisitely sensitive to changes in spatial and temporal frequency (3, 4). Neuronal correlates of visual timing in higher-order visual areas, and potential associations between that activity and the perception of timing, remain unexplored.A major consideration when studying primate vision is that it is interrupted by saccadic eye movements. Consequently, each "snapshot" of the visual world, during an intersaccadic interval, is less than a half-second long (5). The accurate perception of time intervals at such brief timescales is important in itself (e.g., for estimating the speed of briefly appearing objects) and is elemental for longer timing judgments that span multiple saccades. However, despite a growing interest in time estimation in the visual system (6), few experiments have studied it at subsecond timescales.Our overall goal was to determine the relationship between neuronal activity and the perception of visual timing at subsecond timescales. The simplest possibility is that the latency of sensory responses dictates subsecond temporal perception. However, this straightforward hypothesis is complicated by the fact that visual time perception can vary on the order of tens to hundreds o...

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Section: Discussioncontrasting

confidence: 96%

Neuronal correlates of visual time perception at brief timescales

Mayo

Sommer

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…This may explain why previous studies have reported results of perceptual decision-related activity in the motor cortex (Donner et al, 2009) or in the corticostriatal network, which is thought to be related to action selection (Forstmann et al, 2010). However, studies that dissociated the perceptual decision from the response modality have observed neural activity in parietal (Bennur and Gold, 2011) and prefrontal (Heekeren et al, 2006;Ferrera et al, 2009) cortices, regions that may be more related to the perceptual decision itself rather than motor preparation. In our experiment, we have carefully minimized the possibility that our results would be contaminated by motor preparation, by informing subjects of the response mapping only after the presentation of the stimulus.…”

Section: Perceptual Decisions and Motor Preparationmentioning

confidence: 99%

“…Perceptual decision making has recently received great attention by researchers (Heekeren et al, 2008;Ratcliff and McKoon, 2008;Tosoni et al, 2008;Donner et al, 2009;Ferrera et al, 2009;Egner et al, 2010;Noppeney et al, 2010). Perceptual decisions are almost always informed and heavily biased by our prior expectations.…”

Section: Introductionmentioning

confidence: 99%

Prior Expectation Modulates the Interaction between Sensory and Prefrontal Regions in the Human Brain

Rahnev

Lau²,

Lange³

2011

Journal of Neuroscience

129

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How do expectations about the identity of a forthcoming visual stimulus influence the neural mechanisms of perceptual decision making in the human brain? Previous investigations into this issue have mostly involved changing the subjects' attentional focus or the behavioral relevance of certain targets but rarely manipulated subjects' prior expectation about the likely identity of the stimulus. Also, because perceptual decisions were often paired with specific motor responses, it has been difficult to dissociate neural activity that reflects perceptual decisions from motor preparatory activity. Here we designed a task in which we induced prior expectations about the direction of a moving-dot pattern and withheld the stimulus-response mapping until the subjects were prompted to respond. In line with current models of perceptual decision making, we found that subjects' performance was influenced by their expectation about upcoming motion direction. The integration of such information into the decision process was reflected by heightened activity in the dorsolateral prefrontal cortex. Activity in this area reflected the degree to which subjects adjusted their decisions based on the prior expectation cue. Furthermore, there was increased effective connectivity between sensory regions (motion-sensitive medial temporal area MTϩ) and dorsolateral prefrontal cortex when subjects had a prior expectation about the upcoming motion direction. Dynamic causal modeling suggested that stimulus expectation modulated both the feedforward and feedback connectivity between MTϩ and prefrontal cortex. These results provide a mechanism of how prior expectations may affect perceptual decision making, namely by changing neural activity in, and sensory drive to, prefrontal areas.

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“…Although best known for its key role in eye movements (Ferrier, 1874;Robinson and Fuchs, 1969;Schiller et al, 1979;Goldberg and Bushnell, 1981), FEF is also implicated in working memory (Balan and Ferrera, 2003), decision-making (Ferrera et al, 2009), and mechanisms of attention (Moore and Fallah, 2001). Attention has been shown to enhance oscillatory activity originating in FEF (Buschman and Miller, 2009) and the coupling between FEF and area V4 (Gregoriou et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey

Anderson¹,

Kennedy²,

Martin³

2011

Journal of Neuroscience

107

102

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The frontal eye field (FEF) of the primate neocortex occupies a pivotal position in the matrix of inter-areal projections. In addition to its role in directing saccadic eye movements, it is the source of an attentional signal that modulates the activity of neurons in extrastriate and parietal cortex. Here, we tested the prediction that FEF preferentially excites inhibitory neurons in target areas during attentional modulation. Using the anterograde tracer biotinylated dextran amine, we found that the projections from FEF terminate in all cortical layers of area 46, lateral intraparietal area (LIP), and visual area V4. Axons in layer 1 spread extensively, those in layer 2/3 were most numerous, individual axons in layer 4 formed sprays of collaterals, and those of the deep layers were the finest caliber and irregular. All labeled synapses were the typical asymmetric morphology of excitatory synapses of pyramidal neurons. Dendritic spines were the most frequent synaptic target in all areas (95% in area 46, 89% in V4, 84% in LIP, 78% intrinsic local FEF). The remaining targets were one soma and dendritic shafts, most of which showed characteristics of inhibitory neurons with smooth dendrites (5% of all targets in area 46, 2% in V4, 9% in LIP, and 13% in FEF).

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Frontal eye field neurons signal changes in decision criteria

Cited by 83 publications

References 26 publications

Neuronal correlates of visual time perception at brief timescales

Neuronal correlates of visual time perception at brief timescales

Prior Expectation Modulates the Interaction between Sensory and Prefrontal Regions in the Human Brain

Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey

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