POD06 Human pedunculopontine nucleus displays vestibular reactivity

Abstract

We recorded local field potentials (LFPs) in a patient with implanted bilateral subthalamic nucleus (STN) and pedunculopontine nucleus (PPN) deep brain stimulation (DBS) electrodes at 2 kHz and filtered at 0.5–500 Hz. Frequency power spectra and the average power across a 1–100 Hz frequency range was calculated at rest and during passive, yaw-plane whole body rotations at 0.2 Hz and 0.4 Hz with eyes closed and then open with manifest vestibular ocular reflex activation (i.e., nystagmus) and then with eyes open but with VOR suppression (VORS). PPN LFPs showed significant modulation during vestibular activation (rotations) compared to rest with power changes circa four times larger than those found in the STN. The PPN LFP was dominated by theta (4–7 Hz) activity which was enhanced during all tasks compared to rest (including eyes open vs closed at rest) except for VORS where there was a clear reduction in theta activity and this was more prominent for fast rotations. The pattern of theta activity was the same for right and left PPN including task-dependent modulation. In summary, our data show that human PPN activity in the theta range is increased by visual and vestibular input except during VORS when there is a prominent attenuation of theta activity. An attenuation of neural activity is known to occur in primate brainstem circuits mediating the VOR during VOR suppression. Our data thus suggest a prominent role for vestibular signals in PPN functioning.

Vestibular pathways involved in cognition

“…Vestibular inputs are known to project to both the PPTg and reticularis pontis oralis (Vertes and Kocsis, 1997; Bland and Oddie, 1998; Seemungal et al, 2010; Aravamuthan and Angelaki, 2012). The influence of the vestibular system seems important as 72.5% of the PPTg’s neurons in monkeys respond to vestibular stimulation (rotation or translation) (Aravamuthan and Angelaki, 2012).…”

“…In this system the PPTg appears to modulate the reticularis pontis oralis activity through direct cholinergic projections (Shiromani et al, 1988 ; Semba and Fibiger, 1992 ; Vertes and Kocsis, 1997 ). Vestibular inputs are known to project to both the PPTg and reticularis pontis oralis (Vertes and Kocsis, 1997 ; Bland and Oddie, 1998 ; Seemungal et al, 2010 ; Aravamuthan and Angelaki, 2012 ). The influence of the vestibular system seems important as 72.5% of the PPTg’s neurons in monkeys respond to vestibular stimulation (rotation or translation) (Aravamuthan and Angelaki, 2012 ).…”

The modulation of hippocampal theta rhythm by the vestibular system

“…The PPTg projects to the RPO, SUM, the septum, substantia nigra, lateral hypothalamus, median raphe nucleus, medial thalamic and intralaminar thalamic nuclei (Woolf and Butcher 1989;Bland and Oddie 1998;Semba and Fibiger 1992;Pahapill and Lozano 2000;Pignatelli et al 2012). Both the PPTg and RPO respond to vestibular stimulation (Aravamuthan and Angelaki 2012;Bland and Oddie 1998;Seemungal et al 2010;Vertes and Kocsis 1997). When either the RPO or PPTg is stimulated, hippocampal theta is elicited, with increased stimulation producing a linear increase in theta frequency (Bland and Oddie 1998; Kinney et al 1998;Klemm 1972;McNaughton and Sedgwick 1978;Oddie et al 1994;Vertes and Kocsis 1997).…”

Low-intensity vestibular noise stimulation improves postural symptoms in progressive supranuclear palsy

“…The PPN, a central neuronal hub along this pathway, provides the primary cholinergic input to the thalamus. Natural vestibular input as well as vestibular neuromodulation via nGVS were shown to directly modulate PPN activity in animal models and humans [ 1 , 10 , 49 ]. In PSP, neuronal loss in the PPN and the thalamus is a common and early neurodegenerative sign in the course of disease [ 22 , 29 , 59 , 68 ], which entails a substantial reduction of thalamic cholinergic activity in afflicted patients [ 23 ].…”