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. 2003 Dec 17;23(37):11577-86.
doi: 10.1523/JNEUROSCI.23-37-11577.2003.

Cortical representation of bimanual movements

Uri Rokni  1 , Orna Steinberg, Eilon Vaadia, Haim Sompolinsky
Affiliations

Cortical representation of bimanual movements

Uri Rokni et al. J Neurosci. .

Abstract

It is well established that the discharge of neurons in primate motor cortex is tuned to the movement direction of the contralateral arm. Interestingly, it has been found that these neurons exhibit a directional tuning to the ipsilateral arm as well and that the preferred directions to both arms tend to be similar. A recent study showed that motor cortex cells are also directionally selective to bimanual movements, but the relationship between the bimanual and unimanual representations remains unclear. To address this issue, we analyzed the responses of motor cortical neurons recorded from two macaque monkeys during unimanual and bimanual reaching movements. We decomposed the bimanual movement representation into contralateral and ipsilateral directionally tuned components. Our major finding is that the movement of the contralateral arm modifies the tuning of the cells to the ipsilateral arm such that: (1) the offset and modulation depth of the tuning are suppressed; and (2) the preferred directions are randomly shifted. Both these effects eliminate the correlation between the contralateral and ipsilateral representations during bimanual movements. We suggest that the modification of the ipsilateral arm representation is caused by the recruitment of local inhibition that conveys callosal inputs during bimanual movements. This hypothesis is supported by the analysis of a model of two motor cortical networks, coupled with sparse random interhemispheric projections that reproduce the main features observed in the data. Finally, we show that the modification of the ipsilateral arm representation reduces the interference between the movements of both arms.

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Figures

Figure 1.
Figure 1.
Example of directional tuning of one cell from MI. a, Unimanual contralateral (left) and ipsilateral (right) tuning curves (+) and cosine fits (solid lines). b, Bimanual parallel (left) and opposite (right) tuning curves (+), cosine fits (solid lines), and the bimanual cosine tuning expected according to the linear hypothesis (dashed line). c, We obtain the bimanual contralateral (left) and ipsilateral (right) components defined in Equation 9 (solid lines) with PDs θbiC and θbiI, respectively (solid vertical lines), by summing and subtracting the parallel and opposite tuning curves in b, respectively. The dashed lines represent the linear hypothesis prediction.
Figure 2.
Figure 2.
The correlation between the PDs of the contralateral and ipsilateral representations. a, Histogram of differences between the unimanual contralateral PD formula image and the uni-manual ipsilateral PD formula image (bars) and the network model prediction (solid line). b, Histogram of differences between the unimanual contralateral PD formula image and the bimanual ipsilateral PD formula image (bars) and the network model prediction (solid line).
Figure 4.
Figure 4.
The bimanual offsets are smaller than the linear prediction. a, Means of the unimanual contra offsets (C), unimanual ipsilateral offsets (I), bimanual offsets (B), and sum of unimanual offsets (L), over the population of cells. b, Standard deviations of the same sets of offsets as in a. c,d, The predicted means and SDs of the offsets according to the network model.
Figure 5.
Figure 5.
The directional tuning to the movement of one arm is modified when the other arm is moved as well. a, Histogram of the differences between the unimanual PDs and the bimanual PDs (bars), for both contralateral (left) and ipsilateral (right). The solid line depicts the distributions predicted by the network model. b, Scatter plot of the unimanual amplitudes of the cells versus the corresponding bimanual amplitudes (crosses), linear regression of data points (dashed line), and the linear hypothesis prediction (solid line), for both contralateral (left) and ipsilateral (right). The dots depict a sample of 61 cells from the network model.
Figure 7.
Figure 7.
The single-cell and network model predictions on the relationship between the shift of the bimanual ipsilateral PDs (y-axis) and the difference between the two unimanual PDs (x-axis). a, The single-cell model prediction. b, The network model prediction (dots) and the data (crosses).
Figure 8.
Figure 8.
The callosal inhibition mechanism. a, An example of an excitatory cell (light cell) that receives an instruction input that codes for the contralateral arm and a single callosal input that codes for the ipsilateral arm. The callosal input is conveyed by a direct excitatory pathway and via a local inhibitory interneuron (dark cell). The numbers indicate the connection weights. b, The excitatory callosal inputs, inhibitory callosal inputs, and total callosal inputs during unimanual movements (Uni) and during bimanual movements (Bi). c, An example of a cell that receives two callosal inputs. d, The callosal inputs from two sources and their sum during unimanual movements (Uni) and during bimanual movements (Bi). e, The callosal inhibition mechanism is incorporated into a model of two coupled networks, each including an excitatory and inhibitory population of cells.
Figure 9.
Figure 9.
Behavior of the network model. a, The mean shift in the ipsilateral PD versus the heterogeneity index, which quantifies the width of the connection strength distribution. The heterogeneity index is defined as half the distribution width, normalized by the mean connection strength 0.25. b, Gain J of the inhibitory cells versus the mean shift of the ipsilateral PD (solid line) and the correlation between the ipsilateral and contralateral representations (dashed line). This correlation is defined as the mean of formula image. c, The suppression factor of the ipsilateral amplitudes versus J. The suppression factor is defined as the ratio between the mean of formula image and the mean of formula image. d, Mean ipsi PD shift versus the intrahemispherical feeback strength w for J = 0.2.
Figure 3.
Figure 3.
Predictions of the bimanual tuning assumption (Eq. 9). a, The offsets of the parallel tuning curves versus the offsets of the opposite tuning curves (crosses) and the prediction of Equation 9 (solid line). b, The prediction of the tuning to bimanual movements in orthogonal directions when the parallel and opposite tuning curves have the same amplitude and a PD difference of 0°, 90°, and 180°.
Figure 6.
Figure 6.
The single-cell mechanism. The input during a bimanual movement is the sum of the inputs during the two constituent unimanual movements. The nonlinearity of the bimanual response arises from output nonlinearity and causes a negligible PD shift.
Figure 10.
Figure 10.
The modification of the arm representation during bimanual movements implies bimanual decoupling. a, We consider a bimanual movement of the left hand upward and the right hand rightward. b, The bimanual coupling in the absence of the control signal (left) and in the presence of the control signal (right). The population vectors in both cases (total PV) are composed of a contribution of the contralateral components of the bimanual responses (vertical vectors) and a contribution of the ipsilateral components (horizontal vectors). The lines represent the populations of vectors. c, The error in the direction of movement can be continuously modulated by the control signal.
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