scholarly journals The eyes reflect an internal cognitive state hidden in the population activity of cortical neurons

Author(s):  
Richard Johnston ◽  
Adam C. Snyder ◽  
Sanjeev B. Khanna ◽  
Deepa Issar ◽  
Matthew A. Smith

SummaryDecades of research have shown that global brain states such as arousal can be indexed by measuring the properties of the eyes. Neural signals from individual neurons, populations of neurons, and field potentials measured throughout much of the brain have been associated with the size of the pupil, small fixational eye movements, and vigor in saccadic eye movements. However, precisely because the eyes have been associated with modulation of neural activity across the brain, and many different kinds of measurements of the eyes have been made across studies, it has been difficult to clearly isolate how internal states affect the behavior of the eyes, and vice versa. Recent work in our laboratory identified a latent dimension of neural activity in macaque visual cortex on the timescale of minutes to tens of minutes. This ‘slow drift’ was associated with perceptual performance on an orientation-change detection task, as well as neural activity in visual and prefrontal cortex (PFC), suggesting it might reflect a shift in a global brain state. This motivated us to ask if the neural signature of this internal state is correlated with the action of the eyes in different behavioral tasks. We recorded from visual cortex (V4) while monkeys performed a change detection task, and the prefrontal cortex, while they performed a memory-guided saccade task. On both tasks, slow drift was associated with a pattern that is indicative of changes in arousal level over time. When pupil size was large, and the subjects were in a heighted state of arousal, microsaccade rate and reaction time decreased while saccade velocity increased. These results show that the action of the eyes is associated with a dominant mode of neural activity that is pervasive and task-independent, and can be accessed in the population activity of neurons across the cortex.

Author(s):  
Benjamin R. Cowley ◽  
Adam C. Snyder ◽  
Katerina Acar ◽  
Ryan C. Williamson ◽  
Byron M. Yu ◽  
...  

AbstractAn animal’s decision depends not only on incoming sensory evidence but also on its fluctuating internal state. This internal state is a product of cognitive factors, such as fatigue, motivation, and arousal, but it is unclear how these factors influence the neural processes that encode the sensory stimulus and form a decision. We discovered that, over the timescale of tens of minutes during a perceptual decision-making task, animals slowly shifted their likelihood of reporting stimulus changes. They did this unprompted by task conditions. We recorded neural population activity from visual area V4 as well as prefrontal cortex, and found that the activity of both areas slowly drifted together with the behavioral fluctuations. We reasoned that such slow fluctuations in behavior could either be due to slow changes in how the sensory stimulus is processed or due to a process that acts independently of sensory processing. By analyzing the recorded activity in conjunction with models of perceptual decision-making, we found evidence for the slow drift in neural activity acting as an impulsivity signal, overriding sensory evidence to dictate the final decision. Overall, this work uncovers an internal state embedded in the population activity across multiple brain areas, hidden from typical trial-averaged analyses and revealed only when considering the passage of time within each experimental session. Knowledge of this cognitive factor was critical in elucidating how sensory signals and the internal state together contribute to the decision-making process.


2015 ◽  
Vol 114 (5) ◽  
pp. 2637-2648 ◽  
Author(s):  
Fabrice Arcizet ◽  
Koorosh Mirpour ◽  
Daniel J. Foster ◽  
Caroline J. Charpentier ◽  
James W. Bisley

When looking around at the world, we can only attend to a limited number of locations. The lateral intraparietal area (LIP) is thought to play a role in guiding both covert attention and eye movements. In this study, we tested the involvement of LIP in both mechanisms with a change detection task. In the task, animals had to indicate whether an element changed during a blank in the trial by making a saccade to it. If no element changed, they had to maintain fixation. We examine how the animal's behavior is biased based on LIP activity prior to the presentation of the stimulus the animal must respond to. When the activity was high, the animal was more likely to make an eye movement toward the stimulus, even if there was no change; when the activity was low, the animal either had a slower reaction time or maintained fixation, even if a change occurred. We conclude that LIP activity is involved in both covert and overt attention, but when decisions about eye movements are to be made, this role takes precedence over guiding covert attention.


2020 ◽  
Author(s):  
Yaelan Jung ◽  
Dirk B. Walther

AbstractNatural scenes deliver rich sensory information about the world. Decades of research has shown that the scene-selective network in the visual cortex represents various aspects of scenes. It is, however, unknown how such complex scene information is processed beyond the visual cortex, such as in the prefrontal cortex. It is also unknown how task context impacts the process of scene perception, modulating which scene content is represented in the brain. In this study, we investigate these questions using scene images from four natural scene categories, which also depict two types of global scene properties, temperature (warm or cold), and sound-level (noisy or quiet). A group of healthy human subjects from both sexes participated in the present study using fMRI. In the study, participants viewed scene images under two different task conditions; temperature judgment and sound-level judgment. We analyzed how different scene attributes (scene categories, temperature, and sound-level information) are represented across the brain under these task conditions. Our findings show that global scene properties are only represented in the brain, especially in the prefrontal cortex, when they are task-relevant. However, scene categories are represented in the brain, in both the parahippocampal place area and the prefrontal cortex, regardless of task context. These findings suggest that the prefrontal cortex selectively represents scene content according to task demands, but this task selectivity depends on the types of scene content; task modulates neural representations of global scene properties but not of scene categories.


2016 ◽  
Vol 23 (5) ◽  
pp. 529-541 ◽  
Author(s):  
Sara Ajina ◽  
Holly Bridge

Damage to the primary visual cortex removes the major input from the eyes to the brain, causing significant visual loss as patients are unable to perceive the side of the world contralateral to the damage. Some patients, however, retain the ability to detect visual information within this blind region; this is known as blindsight. By studying the visual pathways that underlie this residual vision in patients, we can uncover additional aspects of the human visual system that likely contribute to normal visual function but cannot be revealed under physiological conditions. In this review, we discuss the residual abilities and neural activity that have been described in blindsight and the implications of these findings for understanding the intact system.


2017 ◽  
Vol 118 (5) ◽  
pp. 2579-2591 ◽  
Author(s):  
Mahmood S. Hoseini ◽  
Jeff Pobst ◽  
Nathaniel Wright ◽  
Wesley Clawson ◽  
Woodrow Shew ◽  
...  

Bursts of oscillatory neural activity have been hypothesized to be a core mechanism by which remote brain regions can communicate. Such a hypothesis raises the question to what extent oscillations are coherent across spatially distant neural populations. To address this question, we obtained local field potential (LFP) and membrane potential recordings from the visual cortex of turtle in response to visual stimulation of the retina. The time-frequency analysis of these recordings revealed pronounced bursts of oscillatory neural activity and a large trial-to-trial variability in the spectral and temporal properties of the observed oscillations. First, local bursts of oscillations varied from trial to trial in both burst duration and peak frequency. Second, oscillations of a given recording site were not autocoherent; i.e., the phase did not progress linearly in time. Third, LFP oscillations at spatially separate locations within the visual cortex were more phase coherent in the presence of visual stimulation than during ongoing activity. In contrast, the membrane potential oscillations from pairs of simultaneously recorded pyramidal neurons showed smaller phase coherence, which did not change when switching from black screen to visual stimulation. In conclusion, neuronal oscillations at distant locations in visual cortex are coherent at the mesoscale of population activity, but coherence is largely absent at the microscale of the membrane potential of neurons. NEW & NOTEWORTHY Coherent oscillatory neural activity has long been hypothesized as a potential mechanism for communication across locations in the brain. In this study we confirm the existence of coherent oscillations at the mesoscale of integrated cortical population activity. However, at the microscopic level of neurons, we find no evidence for coherence among oscillatory membrane potential fluctuations. These results raise questions about the applicability of the communication through coherence hypothesis to the level of the membrane potential.


Author(s):  
R. Oz ◽  
H. Edelman-Klapper ◽  
S. Nivinsky-Margalit ◽  
H. Slovin

AbstractIntra cortical microstimulation (ICMS) in the primary visual cortex (V1) can generate the visual perception of phosphenes and evoke saccades directed to the stimulated location in the retinotopic map. Although ICMS is widely used, little is known about the evoked spatio-temporal patterns of neural activity and their relation to neural responses evoked by visual stimuli or saccade generation. To investigate this, we combined ICMS with Voltage Sensitive Dye Imaging in V1 of behaving monkeys and measured neural activity at high spatial (meso-scale) and temporal resolution. Small visual stimuli and ICMS evoked population activity spreading over few mm that propagated to extrastriate areas. The population responses evoked by ICMS showed faster dynamics and different spatial propagation patterns. Neural activity was higher in trials w/saccades compared with trials w/o saccades. In conclusion, our results uncover the spatio-temporal patterns evoked by ICMS and their relation to visual processing and saccade generation.


2015 ◽  
Vol 8 (2) ◽  
Author(s):  
Sangil Lee ◽  
Minho Lee ◽  
Hyeonggyu Park ◽  
Mun-Seon Chang ◽  
Ho-Wan Kwak

The goal of the present study was to examine whether intention type affects eye movement patterns in a change detection task In addition, we assessed whether the eye movement index could be used to identify human implicit intent. We attempted to generate three types of intent amongst the study participants, dividing them into one of three conditions; each condition received different information regarding an impending change to the visual stimuli. In the “navigational intent” condition, participants were asked to look for any interesting objects, and were not given any more information about the impending change. In the “low-specific intent” condition, participants were informed that a change would occur. In the “high-specific intent” condition, participants were told that a change would occur, and that an object would disappear. In addition to this main change detection task, participants also had to perform a primary task, in which they were required to name aloud the colors of objects in the pre-change scene. This allowed us to control for the visual searching process during the pre-change scene. The main results were as follows: firstly, the primary task successfully controlled for the visual search process during the pre-change scene, establishing that there were no differences in the patterns of eye movements across all three conditions despite differing intents. Secondly, we observed significantly different patterns of eye movement between the conditions in the post-change scene, suggesting that generating a specific intent for change detection yields a distinctive pattern of eye-movements. Finally, discriminant function analysis showed a reasonable classification rate for identifying a specific intent. Taken together, it was found that both participant intent and the specificity of information provided to the participants affect eye movements in a change detection task.


2019 ◽  
Vol 116 (30) ◽  
pp. 15210-15215 ◽  
Author(s):  
Emily R. Oby ◽  
Matthew D. Golub ◽  
Jay A. Hennig ◽  
Alan D. Degenhart ◽  
Elizabeth C. Tyler-Kabara ◽  
...  

Learning has been associated with changes in the brain at every level of organization. However, it remains difficult to establish a causal link between specific changes in the brain and new behavioral abilities. We establish that new neural activity patterns emerge with learning. We demonstrate that these new neural activity patterns cause the new behavior. Thus, the formation of new patterns of neural population activity can underlie the learning of new skills.


2018 ◽  
Author(s):  
Nikolas A. Francis ◽  
Susanne Radtke-Schuller ◽  
Jonathan B. Fritz ◽  
Shihab A. Shamma

AbstractTask-related plasticity in the brain is triggered by changes in the behavioral meaning of sounds. We investigated plasticity in ferret dorsolateral frontal cortex (dlFC) during an auditory reversal task to study the neural correlates of proactive interference, i.e., perseveration of previously learned behavioral meanings that are no longer task-appropriate. Although the animals learned the task, target recognition decreased after reversals, indicating proactive interference. Frontal cortex responsiveness was consistent with previous findings that dlFC encodes the behavioral meaning of sounds. However, the neural responses observed here were more complex. For example, target responses were strongly enhanced, while responses to non-target tones and noises were weakly enhanced and strongly suppressed, respectively. Moreover, dlFC responsiveness reflected the proactive interference observed in behavior: target responses decreased after reversals, most significantly during incorrect behavioral responses. These findings suggest that the weak representation of behavioral meaning in dlFC may be a neural correlate of proactive interference.Significance StatementNeural activity in prefrontal cortex (PFC) is believed to enable cognitive flexibility during sensory-guided behavior. Since PFC encodes the behavioral meaning of sensory events, we hypothesized that weak representation of behavioral meaning in PFC may limit cognitive flexibility. To test this hypothesis, we recorded neural activity in ferret PFC, while ferrets performed an auditory reversal task in which the behavioral meanings of sounds were reversed during experiments. The reversal task enabled us study PFC responses during proactive interference, i.e. perseveration of previously learned behavioral meanings that are no longer task-appropriate. We found that task performance errors increased after reversals while PFC representation of behavioral meaning diminished. Our findings suggest that proactive interference may occur when PFC forms weak sensory-cognitive associations.


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