Parallel cortical networks for volitional control of swallowing in humans

A number of studies have demonstrated the involvement of parallel networks in the control of voluntary sequential motor procedures. We sought to deter mine whether a parallel network organization may be found for complex, sequ entially based motor systems that are the product of both voluntary and aut omatic control processes. Specifically, we sought to determine whether the cortical organizational scheme for voluntary repetitive swallowing in adult humans is characterized by a hierarchical dual-projection model or by modu les organized into parallel systems. We utilized functional magnetic resona nce imaging (fMRI) to investigate cortical function during normal swallowin g tasks in eight healthy human adults. Subjects performed both dry (saliva) and bolus (3 ml/bolus of water) swallows. Activation during swallowing tas ks localized to sensorimotor areas (M1, S1, and SMA), S2, premotor cortex, posterior parietal cortex, cingulate gyrus, inferior frontal gyrus, the cer ebellum, the insular cortex, auditory cortex, corpus callosum, and the basa l ganglia and thalamus. Principal components analysis (PCA) of these region s revealed five functional clusters or modules: (1) sensorimotor areas and cingulate gyrus; (2) inferior frontal gyrus, S2, corpus callosum, basal gan glia and thalamus; (3) premotor cortex and posterior parietal cortex; (4) c erebellum; and (5) insula. Analysis of the functional relationship between these areas demonstrated two parallel loops defined by connections to eithe r the cerebellum or insula and connected through the sensorimotor-cingulate , module. Path analysis was performed to test the hypothesis of modules org anized into parallel loops versus a hierarchical dual-projection model cons isting of two separate, singular hierarchical serial pathways from the sens orimotor cortex or insula to the thalamus. These results support the model of modules organized into parallel loops (P=0.8), but not the hierarchical dual-projection model (P<0.0001). Organization of the control of voluntary repetitive swallowing into two parallel systems may confer the ability to e ffectively coordinate and integrate this highly complex sequentially based motor behavior.