Cross-species convergence in pupillary response: understanding human anxiety via non-human primate amygdala lesion

Abstract Few studies have used matched affective paradigms to compare humans and non-human primates. In monkeys with amygdala lesions and youth with anxiety disorders, we examined cross-species pupillary responses during a saccade-based, affective attentional capture task. Given evidence of enhanced amygdala function in anxiety, we hypothesized that opposite patterns would emerge in lesioned monkeys and anxious participants. A total of 53 unmedicated youths (27 anxious, 26 healthy) and 8 adult male rhesus monkeys (Macaca mulatta) completed matched behavioral paradigms. Four monkeys received bilateral excitotoxic amygdala lesions and four served as unoperated controls. Compared to healthy youth, anxious youth exhibited increased pupillary constriction in response to emotional and non-emotional distractors (F(1,48) = 6.28, P = 0.02, η2p = 0.12). Pupillary response was associated significantly with anxiety symptoms severity (F(1,48) = 5.59, P = 0.02, η2p = 0.10). As hypothesized, lesioned monkeys exhibited the opposite pattern i.e. decreased pupillary constriction in response to distractors, compared to unoperated control monkeys (F(1,32) = 24.22, P < 0.001, η2 = 0.33). Amygdala lesioned monkeys and youth with anxiety disorders show opposite patterns of pupil constriction in the context of an affective distractor task. Such findings suggest the presence of altered amygdala circuitry functioning in anxiety. Future lesion and human neuroimaging work might examine the way in which specific amygdala sub-nuclei and downstream circuits mediate these effects.

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Is There Any Difference in Human Pupillary Reaction to Acupuncture between Light- and Dark-Adaptive Conditions?

Acupuncture in Medicine ◽

10.1136/acupmed-2011-010106 ◽

2012 ◽

Vol 30 (2) ◽

pp. 109-112

Author(s):

Hidetoshi Mori ◽

Hiroshi Kuge ◽

Tim Hideaki Tanaka ◽

Yuya Kikuchi ◽

Hiroshi Nakajo ◽

...

Keyword(s):

Dark Adaptation ◽

Light Adaptation ◽

Pupil Diameter ◽

Acupuncture Point ◽

Pupillary Response ◽

Acupuncture Stimulation ◽

Pupillary Responses ◽

Significant Difference ◽

Pupil Constriction ◽

Adaptation Experiment

Objectives To determine if acupuncture stimulation elicits a pupillary response under light adaptation and whether there is any difference in the pupillary response between light and dark adaptation environments during acupuncture stimulation. Methods The participants consisted of 55 healthy individuals who had no known eye diseases or pupil abnormalities. Experiment 1 compared pupillary responses between acupuncture stimulation and no-stimulation groups under light adaptation. Experiment 2 compared pupillary responses to acupuncture between two conditions (dark and light adaptation) with a two-period repeated measurement crossover design. For both experiments the pupil diameter was continuously measured for 3 min before stimulation, during stimulation and for 3 min after stimulation. For all acupuncture stimulation interventions an acupuncture needle was inserted superficially at the TE5 acupuncture point followed by gentle tapping stimulation for 90 s. Results In experiment 1 the pupil diameter was significantly decreased during (p<0.01) and after stimulation (p<0.0001) compared with the pupil diameter before stimulation under light adaptation. No significant difference was noted in the serial changes in pupil diameter in the no-stimulation group. In experiment 2 the pupil diameter was significantly decreased 90 s after stimulation (p<0.05) and 150 s after stimulation (p<0.05) under light adaptation conditions. Furthermore, the pupil diameter was significantly decreased 120 s after stimulation (p<0.05) and 150 s after stimulation (p<0.01) under dark adaptation conditions. No significant difference in the serial changes in pupil diameter was noted between the groups. Conclusions This study shows that pupil constriction occurs following acupuncture stimulation under light adaptation and this response is no different from that seen under dark adaptation.

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Relationships between attention to emotion and anxiety among a community sample of adolescents

Psychological Medicine ◽

10.1017/s0033291720003360 ◽

2021 ◽

pp. 1-12

Author(s):

Benjamin C. Mullin ◽

Jacob B. W. Holzman ◽

Laura Pyle ◽

Emmaly L. Perks ◽

Yaswanth Chintaluru ◽

...

Keyword(s):

Anxiety Disorders ◽

Eye Tracking ◽

Attentional Bias ◽

Community Sample ◽

Full Range ◽

Small Samples ◽

Control Analysis ◽

Attentional Processes ◽

Anxious Youth ◽

Case Control Analysis

Abstract Background Attentional bias to threat has been implicated as a cognitive mechanism in anxiety disorders for youth. Yet, prior studies documenting this bias have largely relied on a method with questionable reliability (i.e. dot-probe task) and small samples, few of which included adolescents. The current study sought to address such limitations by examining relations between anxiety – both clinically diagnosed and dimensionally rated – and attentional bias to threat. Methods The study included a community sample of adolescents and employed eye-tracking methodology intended to capture possible biases across the full range of both automatic (i.e. vigilance bias) and controlled attentional processes (i.e. avoidance bias, maintenance bias). We examined both dimensional anxiety (across the full sample; n = 215) and categorical anxiety in a subset case-control analysis (n = 100) as predictors of biases. Results Findings indicated that participants with an anxiety disorder oriented more slowly to angry faces than matched controls. Results did not suggest a greater likelihood of initial orienting to angry faces among our participants with anxiety disorders or those with higher dimensional ratings of anxiety. Greater anxiety severity was associated with greater dwell time to neutral faces. Conclusions This is the largest study to date examining eye-tracking metrics of attention to threat among healthy and anxious youth. Findings did not support the notion that anxiety is characterized by heightened vigilance or avoidance/maintenance of attention to threat. All effects detected were extremely small. Links between attention to threat and anxiety among adolescents may be subtle and highly dependent on experimental task dimensions.

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Elaborate pupils in skates may help camouflage the eye

10.1101/483172 ◽

2018 ◽

Author(s):

Sean Youn ◽

Corey Okinaka ◽

Lydia M Mäthger

Keyword(s):

Light Intensity ◽

Spatial Frequency ◽

Experimental Evidence ◽

Pupillary Response ◽

Pupil Dilation ◽

Primary Factor ◽

Natural Substrate ◽

Spatial Frequencies ◽

Pupillary Responses ◽

Changing Light

AbstractThe little skate Leucoraja erinacea has elaborately shaped pupils, whose characteristics and functions have not been studied extensively. It has been suggested that such pupil shapes may camouflage the eye; yet, no experimental evidence has been presented to support this claim. Skates are bottom-dwellers that often bury into the substrate with their eyes protruding. If these pupils serve any camouflage function, we expect there to be a pupillary response related to the spatial frequency (“graininess”) of the background against which the eye is viewed. Here, we tested whether skate pupils dilate or constrict in response to background spatial frequency. We placed skates on background substrates with different spatial frequencies and recorded pupillary responses at three light intensities. In experiment 1, the skates’ pupillary response to three artificial checkerboards of different spatial frequencies was recorded. Skates responded to changing light intensity with pupil dilation/constriction; yet, their pupils did not change in response to spatial frequency. In experiment 2, in which skates could bury into three natural substrates with different spatial frequencies, such that their eyes protruded above the substrate, the pupils showed a subtle but statistically significant response to changes in substrate spatial frequency. Given the same light intensity, the smaller the spatial frequency of the natural substrate, the more constricted the pupil. While light intensity is the primary factor determining pupil dilation, these experiments are the first to show that pupils also change in response to background spatial frequency, which suggests that the pupil may aid in camouflaging the eye.

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Pupil Response: A Psychophysiological Measure of Fear during Analogue Desensitization,

Perceptual and Motor Skills ◽

10.1177/00315125890693-254 ◽

1989 ◽

Vol 69 (3-2) ◽

pp. 1351-1367

Author(s):

Robert S. Sturgeon ◽

Leslie M. Cooper ◽

Robert J. Howell

Keyword(s):

Pupil Size ◽

Pupillary Response ◽

Pupil Response ◽

Current Technology ◽

Pupillary Responses

15 highly aroused snake phobics individually constructed fear hierarchies by selecting colored photographs of snakes. Subjects either imagined fear scenes based on their photographs or were exposed to duplicate projected slides during desensitization. Pupillary responses of the Slide Group were also recorded before, during, and after desensitization. Fear of snakes was significantly reduced for both groups within five or fewer desensitization sessions. Changes in pupil size of the Slide Group appear to reflect arousal of fear as well as reduction of fear after treatment. Current technology makes pupillary response a viable psychophysiological measure of fear.

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Pupil Response: A Psychophysiological Measure of Fear during Analogue Desensitization

Perceptual and Motor Skills ◽

10.2466/pms.1989.69.3f.1351 ◽

1989 ◽

Vol 69 (3_suppl) ◽

pp. 1351-1367 ◽

Cited By ~ 4

Author(s):

Robert S. Sturgeon ◽

Leslie M. Cooper ◽

Robert J. Howell

Keyword(s):

Pupil Size ◽

Pupillary Response ◽

Pupil Response ◽

Current Technology ◽

Pupillary Responses

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Disentangling listening effort and memory load beyond behavioural evidence: Pupillary response to listening effort during a concurrent memory task

10.1101/2020.05.04.076588 ◽

2020 ◽

Author(s):

Yue Zhang ◽

Alexandre Lehmann ◽

Mickael Deroche

Keyword(s):

Speech Intelligibility ◽

Memory Load ◽

Pupil Diameter ◽

Memory Task ◽

Pupillary Response ◽

Pupil Dilation ◽

Growth Patterns ◽

Listening Effort ◽

Pupillary Responses ◽

Behavioural Evidence

AbstractRecent research has demonstrated that pupillometry is a robust measure for quantifying listening effort. However, pupillary responses in listening situations where multiple cognitive functions are engaged and sustained over a period of time remain hard to interpret. This limits our conceptualisation and understanding of listening effort in realistic situations, because rarely in everyday life are people challenged by one task at a time. Therefore, the purpose of this experiment was to reveal the dynamics of listening effort in a sustained listening condition using a word repeat and recall task.Words were presented in quiet and speech-shaped noise at different signal-to-noise ratios (SNR). Participants were presented with lists of 10 words, and required to repeat each word after its presentation. At the end of the list, participants either recalled as many words as possible or moved on to the next list. Simultaneously, their pupil dilation was recorded throughout the whole experiment.When only word repeating was required, peak pupil dilation (PPD) was bigger in 0dB versus other conditions; whereas when recall was required, PPD showed no difference among SNR levels and PPD in 0dB was smaller than repeat-only condition. Baseline pupil diameter and PPD followed different growth patterns across the 10 serial positions in conditions requiring recall: baseline pupil diameter built up progressively and plateaued in the later positions (but shot up at the onset of recall, i.e. the end of the list); PPD decreased at a pace quicker than in repeat-only condition.The current findings concur with the recent literature in showing that additional cognitive load during a speech intelligibility task could disturb the well-established relation between pupillary response and listening effort. Both the magnitude and temporal pattern of task-evoked pupillary response differ greatly in complex listening conditions, urging for more listening effort studies in complex and realistic listening situations.

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T88. Human and Non-Human Primate Investigations of Approach-Avoidance Conflict: Relevance to Depression and Anxiety Disorders

Biological Psychiatry ◽

10.1016/j.biopsych.2019.03.411 ◽

2019 ◽

Vol 85 (10) ◽

pp. S162-S163

Author(s):

Diego Pizzagalli ◽

Maria Ironside ◽

Ken-ichi Amemori ◽

Callie McGrath ◽

Min Su Kang ◽

...

Keyword(s):

Anxiety Disorders ◽

Depression And Anxiety ◽

Approach Avoidance ◽

Human Primate

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Background luminance effects on pupil size associated with emotion and saccade preparation

Scientific Reports ◽

10.1038/s41598-020-72954-z ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Yih-Giun Cherng ◽

Talia Baird ◽

Jui-Tai Chen ◽

Chin-An Wang

Keyword(s):

Cognitive Processing ◽

Luminance Level ◽

Pupillary Response ◽

Pupil Dilation ◽

Auditory Stimuli ◽

Background Luminance ◽

Sympathetic Activation ◽

Dark Background ◽

Pupillary Responses ◽

Saccade Preparation

Abstract Pupil dilation is consistently evoked by affective and cognitive processing, and this dilation can result from sympathetic activation or parasympathetic inhibition. The relative contributions of the sympathetic and parasympathetic systems on the pupillary response induced by emotion and cognition may be different. Sympathetic and parasympathetic activity is regulated by global luminance level. Higher luminance levels lead to greater activation of the parasympathetic system while lower luminance levels lead to greater activation of the sympathetic system. To understand the contributions of the sympathetic and parasympathetic nervous systems to pupillary responses associated with emotion and saccade preparation, emotional auditory stimuli were presented following the fixation cue whose color indicated instruction to perform a pro- or anti-saccade while varying the background luminance level. Pupil dilation was evoked by emotional auditory stimuli and modulated by arousal level. More importantly, greater pupil dilation was observed with a dark background, compared to a bright background. In contrast, pupil dilation responses associated with saccade preparation were larger with the bright background than the dark background. Together, these results suggest that arousal-induced pupil dilation was mainly mediated by sympathetic activation, but pupil dilation related to saccade preparation was primarily mediated by parasympathetic inhibition.

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Neural correlates of emotional reactivity and regulation in youth with and without anxiety

10.31234/osf.io/avy85 ◽

2020 ◽

Author(s):

Namita Tanya Padgaonkar ◽

Jessica Uy ◽

Samantha DePasque ◽

Adriana Galván ◽

Tara Peris

Keyword(s):

Emotion Regulation ◽

Anxiety Disorders ◽

Emotion Dysregulation ◽

Emotional Reactivity ◽

Frontal Pole ◽

Neural Basis ◽

Youth Anxiety ◽

Age Dependent ◽

Regulatory Capacity ◽

Anxious Youth

Background: Youth with anxiety disorders struggle with managing emotions relative to peers, but the neural basis of this difference has not been examined. Methods: Youth (Mage=13.6; range=8-17) with (n=37) and without (n=24) anxiety disorders completed a cognitive reappraisal task while undergoing fMRI. Emotional reactivity and regulation, functional activation, and beta-series connectivity were compared across groups. Results: Groups did not differ on emotional reactivity or regulation. However, affect ratings and fronto-limbic activation after viewing aversive imagery (with and without regulation) were higher for anxious youth. Anxious youth did not demonstrate age-dependent changes in regulation, whereas regulation in control youth increased linearly. Stronger amygdala-vmPFC connectivity related to greater anxiety in control youth, but less anxiety in anxious youth. Stronger amygdala-frontal pole connectivity related to worse emotion regulation in control youth, but better emotion regulation in anxious youth. Conclusions: Anxious youth regulate when instructed, but this does not relate to age. Viewing aversive imagery related to heightened negative affect even after reappraisal, accompanied by higher fronto-limbic activation. Emotion dysregulation in youth anxiety disorders may stem from heightened emotionality and potent bottom-up neurobiological responses to aversive stimuli. Findings suggest the importance of treatments focused on both reducing initial emotional reactivity and bolstering regulatory capacity.

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Characteristics of the Pupillary Light Reflex in the Macaque Monkey: Discharge Patterns of Pretectal Neurons

Journal of Neurophysiology ◽

10.1152/jn.2000.84.2.964 ◽

2000 ◽

Vol 84 (2) ◽

pp. 964-974 ◽

Cited By ~ 24

Author(s):

Milton Pong ◽

Albert F. Fuchs

Keyword(s):

Light Intensity ◽

Discharge Rate ◽

Pupillary Response ◽

Pupillary Light Reflex ◽

Physiological Data ◽

Full Field ◽

Light Reflex ◽

Pupillary Light ◽

Pupillary Constriction ◽

Discharge Patterns

Anatomical and physiological data have implicated the pretectal olivary nucleus (PON) as the midbrain relay for the pupillary light reflex in a variety of species. To determine the nature of the discharge of pretectal light reflex relay neurons, we recorded their activity in monkeys that were fixating a stationary spot while a full-field random-dot stimulus was flashed on for 1 s. Based on their discharge patterns, neurons in or near the PON came in two varieties. The most prevalent neuron discharged a burst of spikes 56 ms (on average) after the light came on followed by a sustained rate for the duration of the stimulus (burst-sustained neurons). When the light went off, nearly all neurons (33/34) ceased firing, and then all the neurons with a resting response in the dark ( n = 15) resumed firing. Both the firing rate within the burst and the sustained discharge rate increased with log light intensity and the latency of the burst decreased. The burst and cessation of firing were better aligned with the stimulus occurrence than with the onset of pupillary constriction or dilation. Taken together, these data suggest that burst-sustained neurons respond to the visual stimulus eliciting the pupillary change rather than dictating the metrics of the subsequent pupillary response. Electrical stimulation at the site of four of five burst-sustained neurons elicited pupillary constriction at low stimulus strengths after a latency of ∼100 ms. When the electrode was moved 250 μm away from the burst-sustained neuron, the elicited response disappeared. Reconstructions of the locations of burst-sustained luminance neurons place them in the PON or its immediate vicinity. We suggest that PON burst-sustained neurons constitute the pretectal relay for the pupillary light reflex. A minority of our recorded pretectal neurons discharged a burst of spikes at both light onset and light offset. For most of these transient neurons, neither the burst rate nor the interburst rate was significantly related to light intensity. We conclude that these neurons are not involved in the light reflex but subserve some other pretectal function.

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