Based on 3 parameters characterizing manual performance in 11 macaque monkeys (Table
2), the present study provides evidence that a unilateral permanent lesion of the hand representation in M1 does not induce a systematic and long lasting deficit of motor control for the ipsilesional hand, in contrast to the dramatic deficit observed for the contralesional hand. This conclusion (Figs.
2,
3,
4; Table
2) is in line with the general notion that the corticospinal (CS) projection responsible for fine manual control is largely crossed (about 90% of CS axons decussate) and terminates on distal motoneurons, whereas the uncrossed CS projection exerts its control mostly on proximal and axial muscles (e.g. Brinkman and Kuypers
1973). For each of the three parameters we assessed, there was, however, a minority of monkeys exhibiting a modest (but statistically significant) deficit of manual performance for the ipsilesional hand, limited to a few days immediately following the lesion. How serious are these deficits? For the retrieval score data, significant deficits were found in 4 monkeys (out of 11), limited however to 1–3 daily sessions immediately after the lesion. The extent of the deficit (i.e. the decrease in retrieval score) ranged from 30 to 50%, with the exception of 80% in one monkey on one single daily session. Considering the contact time data, the deficits were also moderate (though significant) but, again, in few monkeys (3 out of 11). Out of the five contact times recorded for each slot orientation in each daily session, most often only a single measurement exceeded the upper confidence limit derived from the pre-lesion period (Fig.
3). In the three monkeys showing a modest deficit, in very rare daily sessions two recorded contact times within the same daily session exceeded the confidence limit (Fig.
3: Mk-RO). However, such cases were limited to one to two daily sessions. The contact time data are thus indicative of a very modest effect of the motor cortex lesion on the ipsilesional hand’s manual dexterity per se (specific precision grip ability). As the majority of contact times remained normal in each daily session, it can be concluded that there is no crucial ipsilateral control of the motor cortex on manual dexterity. The lesion of the motor cortex thus appeared to affect slightly more the retrieval score than the contact time. In other words, the effect of the lesion on the ipsilesional hand was more on components of the task distinct from the manual dexterity itself.
Following this deduction, the effect of the lesion on the ipsilesional hand as assessed with the total time to empty the Brinkman box was more prominent, when present, as observed in three monkeys (Mk-MO, Mk-VA and Mk-SL; see Fig.
4). Indeed, in these three monkeys, the effect lasted at least 20 days and was present in about 50% of daily sessions during this post-lesion time window. This observation is consistent with the notion that the Brinkman box task requires a more precise control of the forelimb posture, as the space to access the slots is more restricted than in the Modified Brinkman Board task. As a consequence, more proximal muscles (in part under the control of the uncrossed CS projection) contribute to performance in the Brinkman box task, which are likely to be more affected by an ipsilateral lesion of the motor cortex than distal muscles specialized for manual dexterity per se. Nevertheless, it remains that the majority of monkeys (8 out of 11) did not exhibit a deficit in the Brinkman box task (Table
2), again supporting the notion that the effect of the lesion on the ipsilesional hand is modest, at least for the behavioral tasks considered in the present study. This conclusion is supported by the observation that the deficits seen for the three parameters (Table
2) are not present systematically in the same three to four monkeys. No monkey showed a deficit of the ipsilesional hand for all three parameters, whereas only three monkeys (Mk-SL, Mk-MO and Mk-VA) showed a deficit for two of the three parameters. Four monkeys exhibited a deficit for only one parameter (Mk-GE, Mk-RO, Mk-BI and Mk-JA). Finally, four monkeys showed no deficits at all, although two of them were not tested for the Brinkman box task (Table
2). Surprisingly, the three monkeys exhibiting deficits of the ipsilesional hand for two of the three parameters were those subjected to anti-Nogo-A antibody treatment. It cannot be ruled out that the presence of the osmotic pumps delivering the antibody during 4 weeks may have contributed, at least in part, and indirectly, to these slight deficits. Considering the monkeys showing deficits of manual performance with the ipsilesional hand for either one or two parameters, there is no obvious correlation with the size and/or the precise position of the lesion (Fig.
1). Moreover, deficits in the ipsilesional hand’s manual performance during the days following the lesion of M1 did not correlate with the presence or absence of enhancement of manual performance of the ipsilesional hand on the long-term, found in the monkeys which recovered best their manual performance for the contralesional hand (Kaeser et al.
2010). Finally, there was no systematic relationship between the deficits observed for the ipsilesional hand in some monkeys for one or two motor parameters (Table
2) and the presence/absence of subcortical lesion in the white matter (Table
1). At the other extreme (no deficit), one animal (Mk-AV) was characterized by a very rostral lesion, located mainly in PM, in line with moderate deficits for the contralesional hand and no deficit for the ipsilesional hand.
The deficits observed in the Brinkman box task (increase in the total time that lasted 20 days) for three monkeys after permanent lesion of the motor cortex (Table
2), and while retrieving the pellets from the horizontal slots for Mk-LA that received a reversible lesion, suggest that the impact of the lesion may be indirect via an effect on the posture of the hand. Indeed, the Brinkman box task requires precision control of the hand posture (wrist muscles) within a restricted space in order to perform the grasping. In Mk-LA, the predominant effect on the horizontal slots is consistent with the notion that grasping is more difficult from the horizontal slots, requiring an additional postural adjustment of the hand, as compared to the vertical slots (see Freund et al.
2009).