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A neural mechanism for exacerbation of headache by light.

Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, Burstein R - Nat. Neurosci. (2010)

Bottom Line: The perception of migraine headache, which is mediated by nociceptive signals transmitted from the cranial dura mater to the brain, is uniquely exacerbated by exposure to light.We found that exacerbation of migraine headache by light is prevalent among blind individuals who maintain non-image-forming photoregulation in the face of massive rod/cone degeneration.The cell bodies and dendrites of such dura/light-sensitive neurons were apposed by axons originating from retinal ganglion cells (RGCs), predominantly from intrinsically photosensitive RGCs, the principle conduit of non-image-forming photoregulation.

View Article: PubMed Central - PubMed

Affiliation: Department of Anesthesia, Boston, Massachusetts, USA.

ABSTRACT
The perception of migraine headache, which is mediated by nociceptive signals transmitted from the cranial dura mater to the brain, is uniquely exacerbated by exposure to light. We found that exacerbation of migraine headache by light is prevalent among blind individuals who maintain non-image-forming photoregulation in the face of massive rod/cone degeneration. Using single-unit recording and neural tract tracing in the rat, we identified dura-sensitive neurons in the posterior thalamus whose activity was distinctly modulated by light and whose axons projected extensively across layers I-V of somatosensory, visual and associative cortices. The cell bodies and dendrites of such dura/light-sensitive neurons were apposed by axons originating from retinal ganglion cells (RGCs), predominantly from intrinsically photosensitive RGCs, the principle conduit of non-image-forming photoregulation. We propose that photoregulation of migraine headache is exerted by a non-image-forming retinal pathway that modulates the activity of dura-sensitive thalamocortical neurons.

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Close apposition between dura/light-sensitive neurons and retinal afferents in LP and Po. (a) Synchronization of neuronal activity (top trace) with the current (bottom trace) delivered by the TMR–dextran filled recording micropipette (see text for detail). (b) Dura/light sensitive units (U1–U4) filled with TMR–dextran (red) and retinal axons labeled anterogradely with CTB (green). Each image represents z-stacking of approximately thirty 1–1.5-μm-thick scans. Arrowheads point to potential axodendritic or axosomatic apposition. Localization of each cell body is marked by a yellow star in the low-power, darkfield inset. Numbers indicate distance from Bregma. (c) Evidence for axodendritic and axosomatic apposition within a single 1–1.5-μm-thick scan taken from the units shown in b. (d) Neuronal firing in response to 50,000 lux of white light (green line and shaded area), corresponding to the individual neurons shown in b. Scale bars represent 50 μm (b,c).
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Figure 3: Close apposition between dura/light-sensitive neurons and retinal afferents in LP and Po. (a) Synchronization of neuronal activity (top trace) with the current (bottom trace) delivered by the TMR–dextran filled recording micropipette (see text for detail). (b) Dura/light sensitive units (U1–U4) filled with TMR–dextran (red) and retinal axons labeled anterogradely with CTB (green). Each image represents z-stacking of approximately thirty 1–1.5-μm-thick scans. Arrowheads point to potential axodendritic or axosomatic apposition. Localization of each cell body is marked by a yellow star in the low-power, darkfield inset. Numbers indicate distance from Bregma. (c) Evidence for axodendritic and axosomatic apposition within a single 1–1.5-μm-thick scan taken from the units shown in b. (d) Neuronal firing in response to 50,000 lux of white light (green line and shaded area), corresponding to the individual neurons shown in b. Scale bars represent 50 μm (b,c).

Mentions: Retinal afferents were traced anterogradely by injecting 6 μl 1% CTB into the vitreous body of one eye under brief isoflurane anesthesia. Three days later, individual dura/light-sensitive neurons (one neuron/rat) were identified in the contralateral posterior thalamus using a recording glass micropipette (20 mˆ) under extended isoflurane anesthesia. A neuron thus identified was then filled with the anterograde tracer tetramethylrhodamine–dextran conjugate (TMR–dextran) which was preloaded into the recording micropipette. Juxtacellular iontophoresis of the tracer into the target neuron was performed over a period of 10–60 min by synchronizing neuronal firing with 1–10 nA positive current delivered in a train of 200-ms on/off intervals (Fig. 3a).


A neural mechanism for exacerbation of headache by light.

Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, Burstein R - Nat. Neurosci. (2010)

Close apposition between dura/light-sensitive neurons and retinal afferents in LP and Po. (a) Synchronization of neuronal activity (top trace) with the current (bottom trace) delivered by the TMR–dextran filled recording micropipette (see text for detail). (b) Dura/light sensitive units (U1–U4) filled with TMR–dextran (red) and retinal axons labeled anterogradely with CTB (green). Each image represents z-stacking of approximately thirty 1–1.5-μm-thick scans. Arrowheads point to potential axodendritic or axosomatic apposition. Localization of each cell body is marked by a yellow star in the low-power, darkfield inset. Numbers indicate distance from Bregma. (c) Evidence for axodendritic and axosomatic apposition within a single 1–1.5-μm-thick scan taken from the units shown in b. (d) Neuronal firing in response to 50,000 lux of white light (green line and shaded area), corresponding to the individual neurons shown in b. Scale bars represent 50 μm (b,c).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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Figure 3: Close apposition between dura/light-sensitive neurons and retinal afferents in LP and Po. (a) Synchronization of neuronal activity (top trace) with the current (bottom trace) delivered by the TMR–dextran filled recording micropipette (see text for detail). (b) Dura/light sensitive units (U1–U4) filled with TMR–dextran (red) and retinal axons labeled anterogradely with CTB (green). Each image represents z-stacking of approximately thirty 1–1.5-μm-thick scans. Arrowheads point to potential axodendritic or axosomatic apposition. Localization of each cell body is marked by a yellow star in the low-power, darkfield inset. Numbers indicate distance from Bregma. (c) Evidence for axodendritic and axosomatic apposition within a single 1–1.5-μm-thick scan taken from the units shown in b. (d) Neuronal firing in response to 50,000 lux of white light (green line and shaded area), corresponding to the individual neurons shown in b. Scale bars represent 50 μm (b,c).
Mentions: Retinal afferents were traced anterogradely by injecting 6 μl 1% CTB into the vitreous body of one eye under brief isoflurane anesthesia. Three days later, individual dura/light-sensitive neurons (one neuron/rat) were identified in the contralateral posterior thalamus using a recording glass micropipette (20 mˆ) under extended isoflurane anesthesia. A neuron thus identified was then filled with the anterograde tracer tetramethylrhodamine–dextran conjugate (TMR–dextran) which was preloaded into the recording micropipette. Juxtacellular iontophoresis of the tracer into the target neuron was performed over a period of 10–60 min by synchronizing neuronal firing with 1–10 nA positive current delivered in a train of 200-ms on/off intervals (Fig. 3a).

Bottom Line: The perception of migraine headache, which is mediated by nociceptive signals transmitted from the cranial dura mater to the brain, is uniquely exacerbated by exposure to light.We found that exacerbation of migraine headache by light is prevalent among blind individuals who maintain non-image-forming photoregulation in the face of massive rod/cone degeneration.The cell bodies and dendrites of such dura/light-sensitive neurons were apposed by axons originating from retinal ganglion cells (RGCs), predominantly from intrinsically photosensitive RGCs, the principle conduit of non-image-forming photoregulation.

View Article: PubMed Central - PubMed

Affiliation: Department of Anesthesia, Boston, Massachusetts, USA.

ABSTRACT
The perception of migraine headache, which is mediated by nociceptive signals transmitted from the cranial dura mater to the brain, is uniquely exacerbated by exposure to light. We found that exacerbation of migraine headache by light is prevalent among blind individuals who maintain non-image-forming photoregulation in the face of massive rod/cone degeneration. Using single-unit recording and neural tract tracing in the rat, we identified dura-sensitive neurons in the posterior thalamus whose activity was distinctly modulated by light and whose axons projected extensively across layers I-V of somatosensory, visual and associative cortices. The cell bodies and dendrites of such dura/light-sensitive neurons were apposed by axons originating from retinal ganglion cells (RGCs), predominantly from intrinsically photosensitive RGCs, the principle conduit of non-image-forming photoregulation. We propose that photoregulation of migraine headache is exerted by a non-image-forming retinal pathway that modulates the activity of dura-sensitive thalamocortical neurons.

Show MeSH
Related in: MedlinePlus