Neuroimaging the brain areas activated by muscle and cutaneous afferents


Experimental setup and stimulus block design. The trial block design consisted of 8 fMRI collection runs. The order of the cutaneous or muscle stimulus blocks as well as the order of stimulus intensity (2T or 4T) were randomized. The different stimulus paradigms started with either a rest period followed by stimulation (A) or an initial stimulus (B) period.

Experimental setup and stimulus block design. The trial block design consisted of 8 fMRI collection runs. The order of the cutaneous or muscle stimulus blocks as well as the order of stimulus intensity (2T or 4T) were randomized. The different stimulus paradigms started with either a rest period followed by stimulation (A) or an initial stimulus (B) period.

Inputs from specialised cutaneous and muscle afferents are crucial for tactile manipulation and accurate movement and postural control.  Both sets of afferents project to the cerebral cortex and contribute to proprioceptive senses (e.g. Proske & Gandevia, 2012).  We used functional magnetic resonance imaging (fMRI) to compare the cortical activation produced by cutaneous versus muscle inputs arising from the same region of the human hand.  We stimulated electrically the digital nerve of the index finger to activate cutaneous (and joint) afferents and we also stimulated over the motor point of the first dorsal interosseous muscle to activate selectively muscle afferents.  Stimuli were also applied at two intensities.  

WHAT DID WE FIND?

We used blood-oxygen-level dependent imaging. Stimulation of both afferent ‘channels’ (i.e. skin or muscle) significantly activated areas in the cortex, areas subcortically, and areas in the cerebellum.  Selective stimulation of muscle afferents activated major motor-related areas.  Compared to the cutaneous stimuli, muscle afferent stimulation caused significantly greater activation within the contralateral precentral gyrus (primary motor cortex), insula, and within the ipsilateral cerebellum, as well as larger areas of reduced blood flow.  Importantly, with muscle afferent stimulation, there was a separate area of precentral and postcentral excitation.  Contrary to the findings obtained by recording evoked potentials with similar stimuli, we found that muscle afferents evoke much more widespread cortical, subcortical, and cerebellar activation than do cutaneous afferents. This emphasises the importance of muscle afferent information and it also means that it is necessary to match joint movement, joint position, and muscle forces in studies of movement in order to avoid the results being confounded by changes in activation of muscle afferents. 

 

Activations in response to muscle stimulation. Group brain activation in response to stimulation of the motor point of the right first dorsal interosseus muscle. The axial/horizontal sections in the upper row show activation areas at the sensorimotor cortex. Sections in the middle row show activation areas in the second sensory area, thalamus, and insula. Sections in the lower row show activation areas in the right and midline cerebellum, including the nucleus (dentate).

Activations in response to muscle stimulation. Group brain activation in response to stimulation of the motor point of the right first dorsal interosseus muscle. The axial/horizontal sections in the upper row show activation areas at the contralateral sensorimotor cortex. Sections in the middle row show activation areas in the second sensory area, thalamus, and insula. Sections in the lower row show activation areas in the right and midline cerebellum, including the dentate nucleus.

SIGNIFICANCE AND IMPLICATIONS

These results provide new insight into the supraspinal projections of human muscle afferents.  Consistent with clinical observations of the impairment of movement produced by sensory loss, our results help to explain the contribution of disturbed sensorimotor processing to disorders of movement.

 

PUBLICATION

Wardman DL, Gandevia SC, Colebatch JG (2014). Cerebral, subcortical, and cerebellar activation evoked by selective stimulation of muscle and cutaneous afferents: an fMRI study. Physiol Reports 2, e00270.

 

KEY REFERENCES

Proske U & Gandevia SC. (2012). The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev 92, 1651-1697.

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