4.7 Article

Differential Activation of the Human Trigeminal Nuclear Complex by Noxious and Non-Noxious Orofacial Stimulation

Journal

HUMAN BRAIN MAPPING
Volume 30, Issue 11, Pages 3772-3782

Publisher

WILEY
DOI: 10.1002/hbm.20805

Keywords

pain; trigeminal; brainstem; muscle; skin; afferent

Ask authors/readers for more resources

There is good evidence from animal studies for segregation in the processing of non-nociceptive and nociceptive information within the trigeminal brainstem sensory nuclear complex. However, it remains unknown whether a similar segregation occurs in humans, and a recent tract tracing study suggests that this segregation may not exist. We used functional magnetic resonance imaging (fMRI) to define and compare activity patterns of the trigeminal brainstem nuclear complex during non-noxious and noxious cutaneous and non-noxious and noxious muscle orofacial stimulation in humans. We found that during cutaneous pain, signal intensity increased within the entire rostrocaudal extent of the spinal trigeminal nucleus (SpV), encompassing the ipsilateral oralis (SpVo), interpolaris (SpVi) and caudalis (SpVc) subdivisions. In contrast, muscle pain did not activate SpVi, but instead activated a discrete region of the ipsilateral SpVo and SpVc. Further, muscle noxious stimulation activated a region of the ipsilateral lateral pons in the region of the trigeminal principal sensory nucleus (Vp). Innocuous orofacial stimulation (lip brushing) also evoked a significant increase in signal intensity in the ipsilateral Vp; however, non-noxious muscle stimulation showed no increase in signal in this area. The data reveal that orofacial cutaneous and muscle nociceptive information and innocuous cutaneous stimulation are differentially represented within the trigeminal nuclear complex. It is well established that cutaneous and muscle noxious stimuli evoke different perceptual, behavioural and cardiovascular changes. We speculate that the differential activation evoked by cutaneous and muscle noxious stimuli within the trigeminal sensory complex may contribute to the neural basis for these differences. Hum Brain Mapp 30:3772-3782, 2009. (C) 2009 Wiley-Liss, Inc.

Authors

I am an author on this paper
Click your name to claim this paper and add it to your profile.

Reviews

Primary Rating

4.7
Not enough ratings

Secondary Ratings

Novelty
-
Significance
-
Scientific rigor
-
Rate this paper

Recommended

Article Clinical Neurology

Alterations in pain processing circuitries in episodic migraine

Tiffani J. Mungoven, Kasia K. Marciszewski, Vaughan G. Macefield, Paul M. Macey, Luke A. Henderson, Noemi Meylakh

Summary: This study found that migraineurs displayed increased activation of the dorsolateral prefrontal cortex (dlPFC) during orofacial heat stimulation, along with reduced connectivity between dlPFC and pain modulatory regions. These findings suggest that the modulation of pain modulatory areas by higher cortical regions may be altered in migraineurs, particularly prior to the onset of a migraine attack.

JOURNAL OF HEADACHE AND PAIN (2022)

Article Neurosciences

Brain activity changes associated with pain perception variability

L. Crawford, E. Mills, N. Meylakh, P. M. Macey, V. G. Macefield, L. A. Henderson

Summary: Pain perception can be modulated by various factors, and individuals show differences in pain ratings and neural circuitry during identical noxious stimulation. Considering variability of baseline pain is important in pain modulatory paradigms, as it affects brain activity and connectivity.

CEREBRAL CORTEX (2023)

Article Neurosciences

The waiting game: investigating the neurobiological transition from acute to persistent pain in adolescent rats

Sabrina Salberg, Angela Doshen, Glenn R. Yamakawa, Jillian Vinall Miller, Melanie Noel, Luke Henderson, Richelle Mychasiuk

Summary: Persistent postsurgical pain affects 20% of youth, with females experiencing chronic pain more than males. This study investigated the neurobiological changes underlying the transition from acute to persistent pain following surgery in adolescence, finding that injury resulted in persistent pain in both sexes, with females displaying greater sensitivity. Gray matter density changes in specific brain areas were observed, driven by different genders. The study emphasizes the importance of studying both sexes and adolescents to better understand postoperative pain.

CEREBRAL CORTEX (2023)

Review Clinical Neurology

Brain and cardiovascular-related changes are associated with aging, hypertension, and atrial fibrillation

Donggyu Rim, Luke A. Henderson, Vaughan G. Macefield

Summary: This study reviews the functional and structural brain changes in healthy aging, hypertension, and atrial fibrillation, noting their potential influence on the autonomic nervous system and cardiovascular control.

CLINICAL AUTONOMIC RESEARCH (2022)

Article Neurosciences

Detailed organisation of the human midbrain periaqueductal grey revealed using ultra-high field magnetic resonance imaging

Fernando A. Tinoco Mendoza, Timothy E. S. Hughes, Rebecca Robertson, Lewis S. Crawford, Noemi Meylakh, Paul M. Macey, Vaughan G. Macefield, Kevin A. Keay, Luke A. Henderson

Summary: The PAG is a critical region for pain-related responses and shows a crude somatotopy for contextually appropriate behavioral responses. Different regions in the PAG are activated by cutaneous and muscle pain. Using ultra-high field functional magnetic resonance imaging, it was found that the PAG exhibits different signal intensity changes in response to noxious stimuli. This suggests a preserved somatotopic organization in the PAG between animals and humans.

NEUROIMAGE (2023)

Letter Respiratory System

Central apnoeas, sympathetic activation and mortality in heart failure: look before you leap

Chiara Borrelli, Jens Spiesshoefer, Vaughan Macefield, Alberto Giannoni

EUROPEAN RESPIRATORY JOURNAL (2022)

Article Physiology

Sensorimotor control in the congenital absence of functional muscle spindles

Vaughan G. G. Macefield, Lyndon J. J. Smith, Lucy Norcliffe-Kaufmann, Jose-Alberto Palma, Horacio Kaufmann

Summary: This review focuses on hereditary sensory and autonomic neuropathy type III (HSAN III).

EXPERIMENTAL PHYSIOLOGY (2023)

Article Peripheral Vascular Disease

Catheter-Based Renal Denervation: 9-Year Follow-Up Data on Safety and Blood Pressure Reduction in Patients With Resistant Hypertension

Gianni Sesa-ashton, Janis M. Nolde, Ida Muente, Revathy Carnagarin, Rebecca Lee, Vaughan G. Macefield, Tye Dawood, Yusuke Sata, Elisabeth A. Lambert, Gavin W. Lambert, Antony Walton, Marcio G. Kiuchi, Murray D. Esler, Markus P. Schlaich

Summary: Long-term follow-up studies on catheter-based renal denervation in patients with resistant hypertension show that the method can still effectively reduce blood pressure and decrease medication usage after nearly 9 years of follow-up, without any adverse effects on renal function.

HYPERTENSION (2023)

Article Neurosciences

How Tactile Afferents in the Human Fingerpad Encode Tangential Torques Associated with Manipulation: Are Monkeys Better than Us?

Alastair J. Loutit, Heather E. Wheat, Heba Khamis, Richard M. Vickery, Vaughan G. Macefield, Ingvars Birznieks

Summary: Dexterous object manipulation relies on force and torque information from tactile afferents in the fingerpads. We compared how human and monkey afferents encode torque information and found differences in response characteristics. Human afferents showed inferior discrimination capacity compared to monkey afferents possibly due to differences in fingertip tissue compliance and skin friction.

JOURNAL OF NEUROSCIENCE (2023)

Article Biology

Stimulus-independent and stimulus-dependent neural networks underpin placebo analgesia responsiveness in humans

Lewis S. Crawford, Noemi Meylakh, Paul M. Macey, Vaughan G. Macefield, Kevin A. Keay, Luke A. Henderson

Summary: An fMRI study with 47 participants has discovered that stimulus-independent and stimulus-dependent neural networks centered around the midbrain periaqueductal gray region are responsible for an individual's ability to experience placebo analgesia. The specific neural circuits that regulate placebo analgesic responsiveness are still unknown, but involvement of brainstem pain modulatory regions is considered crucial. This study demonstrates differences in neural circuit connectivity between placebo responders and non-responders, highlighting the importance of altered connections involving the hypothalamus, anterior cingulate cortex, and midbrain periaqueductal gray matter in the placebo analgesic response.

COMMUNICATIONS BIOLOGY (2023)

Article Neurosciences

Function and biochemistry of the dorsolateral prefrontal cortex during placebo analgesia: how the certainty of prior experiences shapes endogenous pain relief

Lewis S. Crawford, Emily P. Mills, A. Peek, Vaughan G. Macefield, Kevin A. Keay, Luke A. Henderson

Summary: Prior experiences, conditioning cues, and expectations of improvement play important roles in placebo analgesia expression, which is mediated by the dorsolateral prefrontal cortex (DLPFC). This study investigated the biochemistry and function of DLPFC in 38 healthy individuals during placebo analgesia. The results showed that the concentration of glutamate in DLPFC was inversely correlated with pain rating variability, and there was altered functional connectivity between DLPFC and the midbrain periaqueductal gray. These findings suggest that DLPFC is involved in formulating stimulus-response relationships during conditioning and translating them into altered cortico-brainstem functional relationships for placebo analgesia expression.

CEREBRAL CORTEX (2023)

Editorial Material Neurosciences

The unbearable lightness of being opinionated

Vaughan Macefield

JOURNAL OF PHYSIOLOGY-LONDON (2023)

Article Neurosciences

Top-down control of vestibular inputs by the dorsolateral prefrontal cortex

Brendan Mccarthy, Sudipta Datta, Gianni Sesa-Ashton, Rebecca Wong, Luke A. Henderson, Tye Dawood, Vaughan G. Macefield

Summary: This study investigates the modulation of vestibular inputs by electrical stimulation of the dlPFC and finds that concurrent stimulation of the dlPFC and vestibular stimulation can effectively eliminate perceptions of sway and sensations of nausea.

EXPERIMENTAL BRAIN RESEARCH (2023)

Letter Clinical Neurology

Sympathetic vascular transduction and baroreflex sensitivity in the context of severe COPD

Gianni Sesa-Ashton, Vaughan G. Macefield

CLINICAL AUTONOMIC RESEARCH (2023)

Article Neurosciences

Electrical stimulation of the ventromedial prefrontal cortex modulates muscle sympathetic nerve activity and blood pressure

Joe A. Braun, Mariya Patel, Luke A. Henderson, Tye Dawood, Vaughan G. Macefield

Summary: We recently demonstrated that transcranial alternating current stimulation of the dorsolateral prefrontal cortex can modulate muscle sympathetic nerve activity, heart rate, and blood pressure. In this study, we tested the effects of stimulation on the ventromedial prefrontal cortices and found partial entrainment of muscle sympathetic nerve activity, as well as modulation of blood pressure and heart rate. Stimulation of the left ventromedial prefrontal cortices resulted in a significant decrease in mean blood pressure.

CEREBRAL CORTEX (2023)

No Data Available