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A nociceptive stress model of adolescent physical abuse induces contextual fear and cingulate nociceptive neuroplasticities

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Abstract

Adolescent physical abuse impairs emotional development and evokes cingulate pathologies, but its neuronal and circuit substrates are unknown. Conditioning adolescent rabbits with noxious colorectal distension for only 2 h over 3 weeks simulated the human child abuse in amplitude, frequency, and duration. Thermal withdrawal thresholds were unchanged suggesting that sensitized spinal mechanisms may not be operable. Unchanged weight, stools, colorectal histology, and no evidence of abdominal pain argue against tissue injury or irritable bowel syndrome. Contextual fear was amplified as they avoided the site of their abuse. Conditioning impacted anterior cingulate and anterior midcingulate (ACC, aMCC) neuron excitability: (1) more neurons responded to cutaneous and visceral (VNox) noxious stimuli than controls engaging latent nociception (present but not manifest in controls). (2) Rear paw stimulation increased responses over forepaws with shorter onsets and longer durations, while forepaw responses were of higher amplitude. (3) There were more VNox responses with two excitatory phases and longer durations. (4) Some had unique three-phase excitatory responses. (5) Long-duration VNox stimuli did not inhibit neurons as in controls, suggesting the release of an inhibitory circuit. (6) aMCC changes in cutaneous but not visceral nociception confirmed its role in cutaneous nociception. For the first time, we report neuroplasticities that may be evoked by adolescent physical abuse and reflect psychogenic pain: i.e., no ongoing peripheral pain and altered ACC nociception. These limbic responses may be a cognitive trace of abuse and may shed light on impaired human emotional development and sexual function.

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Acknowledgements

We are grateful to Kathleen Sayles in the Department of Pathology at Upstate Medical University for the colorectal histology preparations.

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  1. Cingulum Neurosciences Institute, Manlius, NY, USA

    Brent A. Vogt, Leslie J. Vogt & Robert W. Sikes

  2. Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA

    Brent A. Vogt

  3. Department of Physical Therapy, Northeastern University, Boston, MA, USA

    Robert W. Sikes

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  1. Brent A. Vogt
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Vogt, B.A., Vogt, L.J. & Sikes, R.W. A nociceptive stress model of adolescent physical abuse induces contextual fear and cingulate nociceptive neuroplasticities. Brain Struct Funct 223, 429–448 (2018). https://doi.org/10.1007/s00429-017-1502-3

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