Transient Pupil Dilation after Subsaccadic Microstimulation of Primate Frontal Eye Fields

Lehmann, Sebastian; Corneil, Brian D.

doi:10.1523/jneurosci.4264-15.2016

Cited by 53 publications

(57 citation statements)

References 79 publications

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“…Statistical structure also entrains brain areas beyond visual cortex, including motor and premotor cortex [23]. Here, stimulation, e.g., of the frontal eye fields, induces pupil size changes in macaque monkeys [24, 25]. Alternatively or additionally, modulation of the pupil may be mediated by the superior colliculus [9] or the locus coeruleus [26], whose activity is also known to covary with pupil diameter.…”

Section: Discussionmentioning

confidence: 99%

Pupil diameter tracks statistical structure in the environment

Schwiedrzik

Sudmann

2019

Preprint

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10Pupil diameter determines how much light hits the retina, and thus, how much information is 11 available for visual processing. This is regulated by a brainstem reflex pathway. Here, we investigate 12 whether this pathway is under the control of internal models about the environment. If so, this would 13 allow adjusting pupil dynamics to environmental statistics, and hence optimize information 14 transmission. We manipulate environmental temporal statistics by presenting sequences of images 15 that contain internal temporal structure to humans and macaque monkeys. We then measure whether 16 the pupil tracks this structure not only at the rate that immediately arises from variations in luminance, 17 but also at the rate of higher order statistics that are not available from luminance information alone. 18We find entrainment to environmental statistics in both species during the image sequences. 19Furthermore, pupil entrainment predicts later performance in an offline task that taps into the same 20 internal models. Thus, the dynamics of the pupil are under control of internal models which adaptively 21 match pupil diameter to the temporal structure of the environment, in line with an active sensing 22 account. 23 24

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Section: Discussionmentioning

confidence: 99%

Pupil diameter tracks statistical structure in the environment

Schwiedrzik

Sudmann

2019

Preprint

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“…Pupillary dilatation occurs in non-human primates in response to electrical stimulation of the frontal eye field (Brodmann area 8) during passive viewing tasks 173 ("probe in, probe out" conditions 11 ), and of the superior colliculus 174,175 during passive fixation tasks. One study compared non-human primates with amygdala lesions to healthy controls during a free viewing task; pupillary dilation was similar in both groups, but the pupillary light reflex was diminished in the lesion group 176 (Table 2).…”

Section: Pico 3: Pupillary Changes Associated With Cortical Stimulatimentioning

confidence: 99%

“…Similarly, the superior colliculus sends inputs directly, and indirectly via the mesencephalic cuneiform nucleus, to the Edinger-Westphal nucleus 174 . However, there also exist pathways that connect the locus coeruleus with the superior colliculus directly 173 . Limitations It should be noted that this systematic review has some limitations.…”

Section: Pupillary Constrictionmentioning

confidence: 99%

Peer Review #2 of "Cortical modulation of pupillary function: systematic review (v0.1)"

2019

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Background. The pupillary light reflex is the main mechanism that regulates the pupillary diameter; it is controlled by the autonomic system and mediated by subcortical pathways. In addition, cognitive and emotional processes influence pupillary function due to input from cortical innervation, but the exact circuits remain poorly understood. We performed a systematic review to evaluate the mechanisms behind pupillary changes associated with cognitive efforts and processing of emotions and to investigate the cerebral areas involved in cortical modulation of the pupillary light reflex. Methodology. We searched multiple databases until November 2018 for studies on cortical modulation of pupillary function in humans and non-human primates. Of 8809 papers screened, 258 studies were included. Results. Most investigators focused on pupillary dilatation and/or constriction as an index of cognitive and emotional processing, evaluating how changes in pupillary diameter reflect levels of attention and arousal. Only few tried to correlate specific cerebral areas to pupillary changes, using either cortical activation models (employing micro-stimulation of cortical structures in non-human primates) or cortical lesion models (e.g. investigating patients with stroke and damage to salient cortical and/or subcortical areas). Results suggest involvement of several cortical regions, including the insular cortex (Brodmann areas 13 and 16), the frontal eye field (Brodmann area 8) and the prefrontal cortex (Brodmann areas 11 and 25), and of subcortical structures such as the locus coeruleus and the superior colliculus. Conclusions. Pupillary dilatation occurs with many kinds of mental or emotional processes, following sympathetic activation or parasympathetic inhibition. Conversely, pupillary constriction may occur with anticipation of a bright stimulus (even in its absence) and relies on a parasympathetic activation. All these reactions are controlled by subcortical and cortical structures that are directly or indirectly connected to the brainstem pupillary innervation system.

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“…Pupillary dilatation occurs in non-human primates in response to electrical stimulation of the frontal eye field during passive viewing tasks 167 ("probe in, probe out" conditions 11 ), and of the superior colliculus 168,169 during passive fixation tasks. One study compared non-human primates with amygdala lesions to healthy controls during a free viewing task; pupillary dilation was similar in both groups, but the pupillary light reflex was diminished in the lesion group 170 ( Table 2).…”

Section: Pico 3: Pupillary Changes Associated With Cortical Stimulatimentioning

confidence: 99%

“…Similarly, emotional sounds and images induce a state of arousal, which involves sympathetic activity leading to pupillary dilatation. Cerebral structures involved in vigilance, arousal and attention and responsible for changes in pupillary diameter during cognitive and emotional processes include the locus coeruleus 169,176 , the superior colliculus 168 and multiple regions of the frontal cortex 11,167 (Figure 2). Of these, the locus coeruleus seems to be the most influential mediator of the pupillary light reflex.…”

Section: Pico 4: Pupillary Changes Associated With Cognitive and Emotmentioning

confidence: 99%

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Supplemental Information 1: S1 Protocol and Appendix

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Background. The pupillary light reflex is the main mechanism that regulates the pupillary diameter; it is controlled by the autonomic system and mediated by subcortical pathways. In addition, cognitive and emotional processes influence pupillary function due to input from cortical innervation, but the exact circuits remain poorly understood. We performed a systematic review to evaluate the mechanisms behind pupillary changes associated with cognitive efforts and processing of emotions and to investigate the cerebral areas involved in cortical modulation of the pupillary light reflex. Methodology. We searched multiple databases until November 2018 for studies on cortical modulation of pupillary function in humans and non-human primates. Of 8808 papers screened, 252 studies were included. Results. Most investigators focused on pupillary dilatation as an index of cognitive and emotional processing, evaluating how changes in pupillary diameter reflect levels of attention and arousal. Only few tried to correlate specific cerebral areas to pupillary changes, using either cortical activation models (employing micro-stimulation of cortical structures in non-human primates) or cortical lesion models (e.g. investigating patients with stroke and damage to salient cortical and/or subcortical areas). Results suggest involvement of several cortical regions, including the insular cortex, the frontal eye field and the prefrontal cortex, and of subcortical structures such as the locus coeruleus and the superior colliculus. Conclusions. Pupillary dilatation occurs with many kinds of mental or emotional processes, following sympathetic activation or parasympathetic inhibition. This phenomenon is controlled by several subcortical and cortical structures that are directly or indirectly connected to the brainstem pupillary innervation system.

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Transient Pupil Dilation after Subsaccadic Microstimulation of Primate Frontal Eye Fields

Cited by 53 publications

References 79 publications

Pupil diameter tracks statistical structure in the environment

Pupil diameter tracks statistical structure in the environment

Peer Review #2 of "Cortical modulation of pupillary function: systematic review (v0.1)"

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