Symmetric Sensorimotor Somatotopy

BACKGROUND: Functional imaging has recently been used to investigate detailed somatosensory organization in human cortex. Such studies frequently assume that human cortical areas are only identifiable insofar as they resemble those measured invasively in monkeys. This is true despite the electrophysiological basis of the latter recordings, which are typically extracellular recordings of action potentials from a restricted sample of cells. METHODOLOGY/PRINCIPAL FINDINGS: Using high-resolution functional magnetic resonance imaging in human subjects, we found a widely distributed cortical response in both primary somatosensory and motor cortex upon pneumatic stimulation of the hairless surface of the thumb, index and ring fingers. Though not organized in a discrete somatotopic fashion, the population activity in response to thumb and index finger stimulation indicated a disproportionate response to fingertip stimulation, and one that was modulated by stimulation direction. Furthermore, the activation was structured with a line of symmetry through the central sulcus reflecting inputs both to primary somatosensory cortex and, precentrally, to primary motor cortex. CONCLUSIONS/SIGNIFICANCE: In considering functional activation that is not somatotopically or anatomically restricted as in monkey electrophysiology studies, our methodology reveals finger-related activation that is not organized in a simple somatotopic manner but is nevertheless as structured as it is widespread. Our findings suggest a striking functional mirroring in cortical areas conventionally ascribed either an input or an output somatotopic function

Activation tuning and symmetry in flattened representations of pericentral cortex.

<p>Shown are the same two experiments represented in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0001505#pone-0001505-g003" target="_blank">Figure 3</a>. In each plot the cortex is shown as a 2D surface, oriented in approximate rostrocaudal and lateromedial directions. The top plot shows functional data, representing phase lag according to the reference bar at top, superimposed over MI (rostral) and SI (caudal) voxels in gray, as per the legend used in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0001505#pone-0001505-g002" target="_blank">Figures 2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0001505#pone-0001505-g003" target="_blank">3</a>. (Area 3a, between these regions at the fundus of the central sulcus, is not shown.) The middle plot shows these same data binned into grid cells tiling the pericentral cortex. “Active” grid cells are indicated by the average phase lag across voxels within the bin. Grid cells representing pericentral cortex but lacking any active functional voxels are shown as gray (again, as per the <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0001505#pone-0001505-g002" target="_blank">Fig. 2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0001505#pone-0001505-g003" target="_blank">3</a> legends); cells outside MI and SI are white. The bottom plots depict the degree of similarity between active grid cells lying across from each other an equal distance from the fundus, according to the scale bar immediately above. Pairs of active grid cells with similar phase delays are both colored red; pairs of cells with activity out of phase are colored blue. These examples show widespread functional activity on both sides of the fundus, and indicate that much of this mosaic of activity was mirrored by similar activity on the opposite side of the fundus.</p

Sliding window paradigm.

<p>(A) Pneumatic stimulation was delivered to D1, D2, or D4, via a restricted set of jets within a sliding window of stimulation. (B) Voxels correlated to the reference waveform were assigned one of 12 colors, according to the phase delay giving the maximal correlation. Because the number of jet positions was only four (D1) or six (D2/D4), the color values included interpolated phase lags. (C) The colors corresponded to locations on the digit surface, although the mapping from phase delay to location differed depending on stimulation direction.</p

Muscle synergies evoked by microstimulation are preferentially encoded during behavior

Electrical microstimulation studies provide some of the most direct evidence for the neural representation of muscle synergies. These synergies, i.e., coordinated activations of groups of muscles, have been proposed as building blocks for the construction of motor behaviors by the nervous system. Intraspinal or intracortical microstimulation (ICMS) has been shown to evoke muscle patterns that can be resolved into a small set of synergies similar to those seen in natural behavior. However, questions remain about the validity of microstimulation as a probe of neural function, particularly given the relatively long trains of supratheshold stimuli used in these studies. Here, we examined whether muscle synergies evoked during ICMS in two rhesus macaques were similarly encoded by nearby motor cortical units during a purely voluntary behavior involving object reach, grasp, and carry movements. At each microstimulation site we identified the synergy most strongly evoked among those extracted from muscle patterns evoked over all microstimulation sites. For each cortical unit recorded at the same microstimulation site, we then identified the synergy most strongly encoded among those extracted from muscle patterns recorded during the voluntary behavior. We found that the synergy most strongly evoked at an ICMS site matched the synergy most strongly encoded by proximal units more often than expected by chance. These results suggest a common neural substrate for microstimulation-evoked motor responses and for the generation of muscle patterns during natural behaviors

Microstimulation Activates a Handful of Muscle Synergies

Muscle synergies have been proposed as a mechanism to simplify movement control. Whether these coactivation patterns have any physiological reality within the nervous system remains unknown. Here we applied electrical microstimulation to motor cortical areas of rhesus macaques to evoke hand movements. Movements tended to converge toward particular postures, driven by synchronous bursts of muscle activity. Across stimulation sites, the muscle activations were reducible to linear sums of a few basic patterns—each corresponding to a muscle synergy evident in voluntary reach, grasp, and transport movements made by the animal. These synergies were represented nonuniformly over the cortical surface. We argue that the brain exploits these properties of synergies—postural equivalence, low dimensionality, and topographical representation—to simplify motor planning, even for complex hand movements.National Institute of Neurological Disorders and Stroke (U.S.) (Grant NS44393