Abstract
Premotor areas of primates are specialized cortical regions that can contribute to hand movements by modulating the outputs of the primary motor cortex (M1). The goal of the present work was to study how the supplementary motor area (SMA) located within the same hemisphere [i.e., ipsilateral SMA (iSMA)] or the opposite hemisphere [i.e., contralateral (cSMA)] modulate the outputs of M1. We used paired-pulse protocols with intracortical stimulations in sedated capuchin monkeys. A conditioning stimulus in iSMA or cSMA was delivered simultaneously or before a test stimulus in M1 with different interstimulus intervals (ISIs) while electromyographic activity was recorded in hand and forearm muscles. The pattern of modulation from iSMA and cSMA shared some clear similarities. In particular, both areas predominantly induced facilitatory effects on M1 outputs with shorter ISIs and inhibitory effects with longer ISIs. However, the incidence and strength of facilitatory effects were greater for iSMA than cSMA. We then compared the pattern of modulatory effects from SMA to the ones from the dorsal and ventral premotor cortexes (PMd and PMv) collected in the same series of experiments. Among premotor areas, the impact of SMA on M1 outputs was always weaker than the one of either PMd or PMv, and this was regardless of the hemisphere, or the ISI, tested. These results show that SMA exerts a unique set of modulations on M1 outputs, which could support its specific function for the production of hand movements.NEW & NOTEWORTHY We unequivocally isolated stimulation to either the ipsilateral or contralateral supplementary motor area (SMA) using invasive techniques and compared their modulatory effects on the outputs of primary motor cortex (M1). Modulations from both SMAs shared many similarities. However, facilitatory effects evoked from ipsilateral SMA were more common and more powerful. This pattern differs from the ones of other premotor areas, which suggests that each premotor area makes unique contributions to the production of motor outputs.
Highlights
The refinement of manual skills and the development of complex motor behaviors in primates are associated with the appearance of several premotor areas including the supplementary motor area (SMA), the dorsal premotor cortex (PMd), and the ventral premotor cortex (PMv) (Kaas 2006)
The T-only condition evoked a significant average motor-evoked potentials (MEPs) (Ͼ3 SD above baseline; see MATERIALS AND METHODS) in at least one and up to six muscles of the contralateral arm. These MEPs were more common in the abductor pollicis brevis (APB) (n ϭ 24), FPB (n ϭ 23), extensor digitorum communis (EDC) (n ϭ 20), and extensor carpi ulnaris (ECU) (n ϭ 18) and less common in flexor digitorum superficialis (FDS) (n ϭ 15) and palmaris longus (PL) (n ϭ 11)
As we placed our conditioning stimulation (Cstim) and test stimulation (Tstim) electrodes at cortical sites evoking MEPs in digit or forearm muscles with intracortical microstimulation (ICMS) trains, we found very few significant MEPs in proximal arm muscles (BB ϭ 5 and triceps brachii (TB) ϭ 1)
Summary
The refinement of manual skills and the development of complex motor behaviors in primates are associated with the appearance of several premotor areas including the supplementary motor area (SMA), the dorsal premotor cortex (PMd), and the ventral premotor cortex (PMv) (Kaas 2006). One way premotor areas can uniquely contribute to the production of hand movements is by modulating or shaping the outputs of the primary motor cortex (M1) differently Several studies in both humans and monkeys have examined this “physiological connectivity” between premotor areas and M1 using dual site, paired-pulse protocols with transcranial magnetic stimulation (TMS) and intracortical microstimulation (ICMS). Such experiments reveal how premotor areas can enhance (facilitate) or suppress (inhibit) descending motor outputs from M1 and provide information about how these areas can contribute to the production of movements. The opposite trend was found in the contralateral hemisphere, in which PMd induces more frequent and more powerful facilitatory effects than PMv
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