The influence of sensory afferent input on local motor cortical excitatory circuitry in humans

Abstract

Key pointsr In the human, sensorimotor integration can be investigated using combined sensory and transcranial magnetic stimulation (TMS).r Short latency afferent inhibition (SAI) refers to motor cortical inhibition 20-25ms after median nerve stimulation.r We investigated the influence of SAI on a local excitatory interneuronal motor cortical circuit known as short-interval intracortical facilitation (SICF) and found that, contrary to expectations, SICF was facilitated in the presence of SAI (SICF SAI ); this effect is specific to SICF since there was no effect in control conditions in which SICF was not elicited, and the facilitatory SICF SAI interaction increased with increasing strength of SICF or SAI.r The influence of sensory input on excitatory motor cortical circuitry was similar across different bodily regions, different circuits within motor cortex and across functional states, suggesting that this interaction may have general applicability in sensorimotor integration and motor control.r SAI and SICF were found to correlate between individuals in that those with high SAI were found to have high SICF, and this relationship was maintained when SICF was delivered in the presence of SAI, suggesting an intrinsic relationship between SAI and SICF; these findings are compatible with brain-slice studies of sensorimotor circuitry and add to our understanding of sensorimotor integration.Abstract In human, sensorimotor integration can be investigated by combining sensory input and transcranial magnetic stimulation (TMS). Short latency afferent inhibition (SAI) refers to motor cortical inhibition 20-25 ms after median nerve stimulation. We investigated the interaction between SAI and short-interval intracortical facilitation (SICF), an excitatory motor cortical circuit. Seven experiments were performed. Contrary to expectations, SICF was facilitated in the presence of SAI (SICF SAI ). This effect is specific to SICF since there was no effect at SICF trough 1 when SICF was absent. Furthermore, the facilitatory SICF SAI interaction increased with stronger SICF or SAI. SAI and SICF correlated between individuals, and this relationship was maintained when SICF was delivered in the presence of SAI, suggesting an intrinsic relationship between SAI and SICF in sensorimotor integration. The interaction was present at rest and during muscle contraction, had a broad degree of somatotopic influence and was present in different interneuronal SICF circuits induced by posterior-anterior and anterior-posterior current directions. Our results are compatible with the finding that projections from sensory to motor cortex terminate in both superficial layers where late indirect (I-) waves are thought to originate, as well as deeper layers with more direct effect on pyramidal output. This interaction is likely to be relevant to sensorimotor integration and motor control.

Role of cutaneous and proprioceptive inputs in sensorimotor integration and plasticity occurring in the facial primary motor cortex

“…; Cash et al . ) and that by these connections they mediate the SAI (Porter, ; Tsang et al . , ; Cash et al .…”

“…Proprioceptive facial inputs activate inhibitory circuits involving areas 3a and 2 of contralateral SI (Friedman & Jones, 1981;Allison et al 1991) and bilaterally the secondary somatosensory cortex (SII) and the posterior parietal cortex (PPC) (Allison et al 1991;Forss et al 1994;Chen et al 1999;Karhu & Tesche, 1999;Boakye et al 2000;Sailer et al 2002), at LAI intervals (Chen et al 1999;Classen et al 2000). In line with the idea that LAI and PAS share their underpinning circuits (Russmann et al 2009;Meunier et al 2012), it seems reasonable to suppose that the same LAI-inducing proprioceptive input at short intervals might engage excitatory interneurons in SI and M1 (layers 2/3) mediating PAS-induced LTP-like plasticity (Kaneko et al 1994b;Cash et al 2015), but also SII and PPC. The crucial role of SII for sensory processing and sensorimotor integration in face M1 has been confirmed recently by a fMRI study where the Bell's palsy condition induced significant changes in connectivity in SII (Klingner et al 2014).…”

“…It can be hypothesized that low threshold cutaneous trigeminal inputs activate oligosynaptic circuits which might primarily involve inhibitory connections between areas 3b and 1 of the contralateral primary somatosensory cortex (SI), (Allison et al 1991;Forss et al 1994) and layers 5/6 of M1 (Kaneko et al 1994a,b;Porter, 1996;Classen et al 2000;Tokimura et al 2000;Aronoff et al 2010;Mao et al 2011;Cash et al 2015) and that by these connections they mediate the SAI (Porter, 1996;Tsang et al 2014Tsang et al , 2015Cash et al 2015;Kojima et al 2015;Bailey et al 2016). Proprioceptive facial inputs activate inhibitory circuits involving areas 3a and 2 of contralateral SI (Friedman & Jones, 1981;Allison et al 1991) and bilaterally the secondary somatosensory cortex (SII) and the posterior parietal cortex (PPC) (Allison et al 1991;Forss et al 1994;Chen et al 1999;Karhu & Tesche, 1999;Boakye et al 2000;Sailer et al 2002), at LAI intervals (Chen et al 1999;Classen et al 2000).…”

Reduced Short‐Latency Afferent Inhibition Indicates Impaired Sensorimotor Integrity During Migraine Attacks

“…SAI is observed in the first few milliseconds after the latency of the N20 component of the somatosensory evoked potential. Therefore, most researchers use an ISI of 20‐22 milliseconds assuming that the afferent conduction time from the median nerve at the wrist to the sensorimotor cortex is 20 milliseconds . In this study, ISI between electrical and magnetic stimulation was set at 21 milliseconds and 20 MEPs were obtained in the SAI paradigm.…”

“…Therefore, most researchers use an ISI of 20-22 milliseconds assuming that the afferent conduction time from the median nerve at the wrist to the sensorimotor cortex is 20 milliseconds. 27,28 In this study, ISI between electrical and magnetic stimulation was set at 21 milliseconds and 20 MEPs were obtained in the SAI paradigm. MEPs were visually checked for normality during stimulation.…”