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Identification of discrete functional subregions of the human periaqueductal gray

Significance The periaqueductal gray is a brainstem region that is critical for autonomic regulation and for defensive responses (e.g., “fight,” “flight,” “freeze”). It has been studied extensively in rodents and cats, but less is known about the human periaqueductal gray. The small size and shape of the periaqueductal gray makes it challenging to study using standard noninvasive MRI techniques. We used a high-field strength magnet to examine this region at high resolution while participants viewed emotionally aversive or neutral images. Emotion-related functional activity was concentrated in particular subregions and in ways that are consistent with neurobiological observations in nonhuman animals. This study establishes a technique to uncover the functional architecture of the periaqueductal gray in humans. The midbrain periaqueductal gray (PAG) region is organized into distinct subregions that coordinate survival-related responses during threat and stress [Bandler R, Keay KA, Floyd N, Price J (2000) Brain Res 53 (1):95–104]. To examine PAG function in humans, researchers have relied primarily on functional MRI (fMRI), but technological and methodological limitations have prevented researchers from localizing responses to different PAG subregions. We used high-field strength (7-T) fMRI techniques to image the PAG at high resolution (0.75 mm isotropic), which was critical for dissociating the PAG from the greater signal variability in the aqueduct. Activation while participants were exposed to emotionally aversive images segregated into subregions of the PAG along both dorsal/ventral and rostral/caudal axes. In the rostral PAG, activity was localized to lateral and dorsomedial subregions. In caudal PAG, activity was localized to the ventrolateral region. This shifting pattern of activity from dorsal to ventral PAG along the rostrocaudal axis mirrors structural and functional neurobiological observations in nonhuman animals. Activity in lateral and ventrolateral subregions also grouped with distinct emotional experiences (e.g., anger and sadness) in a factor analysis, suggesting that each subregion participates in distinct functional circuitry. This study establishes the use of high-field strength fMRI as a promising technique for revealing the functional architecture of the PAG. The techniques developed here also may be extended to investigate the functional roles of other brainstem nuclei.