Dissociating motor cortex from the motor

Abstract

During closed-loop control of a brain-computer interface, neurons in the primary motor cortex can be intensely active even though the subject may be making no detectable movement or muscle contraction. How can neural activity in the primary motor cortex become dissociated from the movements and muscles of the native limb that it normally controls? Here we examine circumstances in which motor cortex activity is known to dissociate from movement--including mental imagery, visuo-motor dissociation and instructed delay. Many such motor cortex neurons may be related to muscle activity only indirectly. Furthermore, the integration of thousands of synaptic inputs by individual α-motoneurons means that under certain circumstances even cortico-motoneuronal cells, which make monosynaptic connections to α-motoneurons, can become dissociated from muscle activity. The natural ability of motor cortex neurons under voluntarily control to become dissociated from bodily movement may underlie the utility of this cortical area for controlling brain-computer interfaces.

Figure 1. Spike-triggered averages during different individuated finger and wrist movements

Each column shows averages of rectified EMG from each of nine muscles (rows) triggered from spikes discharged by neuron c0107. Averages in the left column (All) incorporate spikes discharged throughout the recording session. Averages in the remaining columns were formed using spikes discharged only during trials of a particular movement, indicated by the number of the digit (1 = thumb through 5 = little finger, W = wrist) and the direction of movement (f = flexion, e = extension). Sweeps were incorporated in each average only if some EMG activity was present above the noise level. Numbers below each trace indicate the number of sweeps included in that average. All averages have been scaled to fill the same vertical height from their minimal to maximal values. The trigger time is indicated by a vertical line in each column. Spike-triggered averages with highly significant effects are shown in red; those with effects of intermediate significance in cyan; those with no significant effect are black if ≥4000 sweeps were available, but grey if <4000.

Figure 2. Spike-triggered averages during eight behavioural epochs

Each column shows averages of rectified EMG from each of 13 muscles (rows) triggered from spikes discharged by neuron e0035_B during 1 of 8 behavioural epochs. During epochs 1 and 8 the monkey performed a simple hand squeeze task. During epochs 2–7 the monkey was rewarded for coactivating the neuron and a particular muscle in a paradigm termed reinforcement of physiological discharge (RPD). Formatting is the same as for Fig. 1. (Reproduced from Davidson et al. 2007a.)

Figure 3. Variation in the amplitude of spike-triggered average effects: firing rate and ongoing EMG

For two of the muscles illustrated in Fig. 2, ECRB (top) and PL (bottom), the peak percent increase (PPI) of the spike-triggered average effects produced by neuron e0035_B in each of the 8 behavioural epochs has been plotted as a function of the mean neuron firing rate (left) and the mean level of ongoing EMG activity in the muscle (centre). The three-dimensional plot (right) of PPI against both firing rate and ongoing EMG has been rotated to show that for each muscle all 8 points lie close to a single plane (viewed here end on), indicating that for these two neuron–muscle pairs PPI was an approximately linear function of firing rate and ongoing EMG. The values plotted here are averages across measurements of neuron firing rate, ongoing EMG (normalized separately between 0 and 1 for each muscle) and PPI made on the multiple fragment spike-triggered averages from each behavioural epoch (Davidson et al. 2007b). Error bars indicate the standard error of the mean. The colour of the symbols indicates the sequential order of the 8 epochs, from red to white. The shape of the symbols indicates the significance of the effects: triangles – high, squares – intermediate, circles – not significant.

Figure 4. A neuron–muscle pair with throughput in one behavioural epoch but not in another

The same neuron–muscle pair produced a highly significant post-spike facilitation (top row) in one behavioural epoch (left), but no effect during another epoch (right) during the same recording session. For the two epochs, the spike-triggered averages are shown scaled to the same vertical height (above) and again relative to zero EMG activity (below). Numbers inset in the latter give the number of triggers used in the average, the onset latency and the peak width at half-maximum of the post-spike facilitation. The middle and bottom rows show box plots illustrating the distributions (line – median, boxes – 25th to 75th percentile, whiskers – remainder, dots – outliers) of neuron firing rate and ongoing EMG, respectively, in multiple fragments of each epoch. Box plots whose notches overlap do not have different medians (P< 0.05). (Modified from Davidson et al. 2007a.)