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Inhalation of 7.5% carbon dioxide increases alerting and orienting attention network function

Abstract

Rationale

The development of experimental models that readily translate between animals and humans is required to better integrate and clarify the biological, behavioural and cognitive mechanisms that underlie normal fear and pathological anxiety. Inhalation of low concentrations of carbon dioxide (CO2) increases anxiety and autonomic arousal in humans, triggers related behaviours in small animals, and increases selective attention to threat in healthy humans. However the effects on broader cognitive (non-emotional) processes that characterize anxiety are not known.

Objectives

To examine the effect of 7.5 % CO2 inhalation (vs. air) on the efficiency of discrete attention networks implicated in anxiety: alerting (maintaining an alert state), orienting (the selection of information from sensory input) and executive control (resolving cognitive conflict).

Methods

Twenty-three healthy human participants completed a computerized Attention Network Test (ANT) during inhalation of 7.5 % CO2 enriched and normal/medical air. Gas was administered blind to participants with inhalation order counterbalanced across participants. Measures of heart rate, blood pressure and subjective mood/anxiety were obtained at baseline and following each inhalation period.

Results

CO2 inhalation increased anxiety, autonomic arousal and the efficiency of alerting and orienting attention network function. Autonomic response to CO2 correlated with increased orienting; and CO2–induced anxiety, autonomic arousal and orienting network function increased with chronic (trait) anxiety.

Conclusions

Evidence that CO2 modulates attention mechanisms involved in the temporal detection and spatial location of salient stimuli converges with evidence that CO2 triggers fear behaviour in animals via direct innervation of a distributed neural network that facilitates environmental hypervigilance.

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Notes

  1. During each inhalation period participants also completed a short (5 min) word classification task. This task addressed different research questions to those of the present study. Task-order was counter-balanced across participants and did not interact with/moderate the observed effects of CO2 on alerting, orienting and executive attention, reported below (i.e. gas x task-order, Fs < 1, p’s > .86).

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Acknowledgements

We would like to thank M Hotton and C Struthers (University of Bristol) for their help with data collection.

Conflict of Interest

DB has acted as a paid consultant to a number of companies with an interest in anxiety disorders (Eli Lilly, GlaxoSmithKline, Grunenthal, Lundbeck, Pfizer, Servier) and has held grants (on behalf of his employer) from Lundbeck and Pfizer. He has accepted paid speaking engagements in industry supported satellite symposia at international and national meetings organized by Lundbeck, Pfizer and Servier. There are no Conflicts of Interest for MG, AA, MRM.

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Correspondence to Matthew Garner.

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Garner, M., Attwood, A., Baldwin, D.S. et al. Inhalation of 7.5% carbon dioxide increases alerting and orienting attention network function. Psychopharmacology 223, 67–73 (2012). https://doi.org/10.1007/s00213-012-2690-4

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  • DOI: https://doi.org/10.1007/s00213-012-2690-4

Keywords

  • Carbon dioxide
  • Anxiety
  • Cognition
  • Autonomic arousal
  • Attention Network Test
  • Noradrenaline