FMRI detection of BOLD responses in both white and gray matter of spinal cord after optogenetic cortical stimulation

We report the first demonstrations of neural activity detected using functional MRI within both the grey and white matters of the cervical spinal cord of non-human primates in response to stimulation by optogenetic excitation of brain cortex. The right secondary somatosensory cortices (S2) of two squirrel monkeys were transfected with Adeno-associated virus that introduced a light sensitive cation channel (ChR2) into neurons. An optical fiber was inserted to selectively activate excitatory neurons in S2 targets using a blue laser. MR images were acquired of the brain and cervical spine at 9.4 Tesla before, during and after optical excitation. Robust blood oxygenation level dependent (BOLD) signal changes (p <0.05 post FDR correction) were detected at the probe location in S2 region and in multiple connected brain regions as expected. At the same level of significance we also detected robust and focal BOLD signal changes in spinal gray and white matters in response to the light stimulation of S2 cortex. For example, the gray matter of the ipsilateral ventral horn and left and right dorsal horns exhibited a classical BOLD signal hemodynamic response, with peak signal amplitudes of approximately 0.5 - 0.9%. Several white matter tracts also demonstrated robust responses. For example, the right and left spino-cerebellar, left cortico-spinal, and dorsal column tracts showed transient increases in BOLD signal that were comparable to those seen in gray matter, and with similar time courses. These effects may represent both antidromic and orthodromic excitation produced within the neurons that normally carry sensory information to S2.