Long-latency reflexes of elbow and shoulder muscles suggest reciprocal excitation of flexors, reciprocal excitation of extensors, and reciprocal inhibition between flexors and extensors

Abstract

Postural corrections of the upper limb are required in tasks ranging from handling an umbrella in the changing wind to securing a wriggling baby. One complication in this process is the mechanical interaction between the different segments of the arm where torque applied at one joint induces motion at multiple joints. Previous studies have shown the long-latency reflexes of shoulder muscles (50-100 ms after a limb perturbation) account for these mechanical interactions by integrating information about motion of both the shoulder and elbow. It is less clear whether long-latency reflexes of elbow muscles exhibit a similar capability and what is the relation between the responses of shoulder and elbow muscles. The present study utilized joint-based loads tailored to the subjects' arm dynamics to induce well-controlled displacements of their shoulder and elbow. Our results demonstrate that the long-latency reflexes of shoulder and elbow muscles integrate motion from both joints: the shoulder and elbow flexors respond to extension at both joints, whereas the shoulder and elbow extensors respond to flexion at both joints. This general pattern accounts for the inherent flexion-extension coupling of the two joints arising from the arm's intersegmental dynamics and is consistent with spindle-based reciprocal excitation of shoulder and elbow flexors, reciprocal excitation of shoulder and elbow extensors, and across-joint inhibition between the flexors and extensors.

Compensating for intersegmental dynamics across the shoulder, elbow, and wrist joints during feedforward and feedback control

“…Many studies have shown that the nervous system accounts for the limb's intersegmental dynamics during self-initiated (i.e., feedforward) control of the arm (Almeida et al 1995;Cooke and Virji-Babul 1995;Corcos et al 1989;Galloway and Koshland 2002;Gottlieb 1998;Gribble and Ostry 1999;Gritsenko et al 2011;Hollerbach and Flash 1982;Koshland et al 1991;Pigeon et al 2003Pigeon et al , 2013Sainburg et al 1995Sainburg et al , 1999Virji-Babul and Cooke 1995). A related series of studies has demonstrated that this capacity is also present during reflexive (i.e., feedback) control of the arm (Crevecoeur et al 2012;Kurtzer et al 2008Kurtzer et al , 2009Kurtzer et al , 2014Kurtzer et al , 2016Lacquaniti and Soechting 1984, 1986a, 1986bPruszynski et al 2011;Soechting and Lacquaniti 1988). For example, Soechting and Lacquaniti (1988) investigated rapid feedback responses following mechanical perturbations at the shoulder and elbow joints when both joints were free to move.…”

“…The loss of somatosensory feedback impairs the nervous system's ability to account for the mechanical interactions between limb segments (Sainburg et al 1995(Sainburg et al , 1999. Indeed, several groups have investigated whether rapid feedback responses (i.e., reflexes) are modulated in a way that accounts for these mechanical interactions (Crevecoeur et al 2012;Kurtzer et al 2008Kurtzer et al , 2009Kurtzer et al , 2014Kurtzer et al , 2016Lacquaniti and Soechting 1984, 1986a, 1986bPruszynski et al 2011;Soechting and Lacquaniti 1988). For example, Kurtzer et al (2008) applied a combination of shoulder and elbow torque perturbations that led to minimal shoulder motion but different amounts of elbow motions.…”

Long-latency reflexes for inter-effector coordination reflect a continuous state feedback controller

“…These are just two of many examples (to be treated in detail later) that provide unambiguous evidence for a MIMO structure in the neural controller. The following is a brief accounting of more of these studies: wrist LLRs dependent on elbow information (Koshland et al 1991;Latash 2000;Weiler et al 2016), wrist LLRs dependent on other wrist muscles (Cody and Plant 1989), elbow LLRs dependent on wrist information (Kurtzer et al 2016), elbow LLRs dependent on shoulder information (Kurtzer et al 2016), elbow LLRs dependent on contralateral elbow information (Dimitriou et al 2012), shoulder LLRs dependent on wrist information (Maeda et al 2017), shoulder LLRs dependent on elbow information (Kurtzer et al 2008(Kurtzer et al , 2009, ankle LLRs dependent on knee and hip information (Safavynia and Ting 2013a), and ankle LLRs dependent on shoulder and elbow information (Lowrey et al 2017).…”

Shared internal models for feedforward and feedback control of arm dynamics in non-human primates

“…Our monkey tasks were chosen in a way to mimic several aspects of previous human studies. First, research has demonstrated that humans generate predictive shoulder muscle activity when generating pure elbow movements (Gribble & Ostry, 1999;Debicki & Gribble, 2005;Maeda et al , 2017Maeda et al , , 2018 and show robust shoulder long-latency reflex responses to perturbations applied to the arm that creates pure elbow motion (Kurtzer, Pruszynski, et al , 2006;Kurtzer et al , 2008Kurtzer et al , , 2009Kurtzer et al , , 2014Kurtzer et al , , 2016Crevecoeur et al , 2012;Maeda et al , 2017Maeda et al , , 2018Kurtzer, 2019;Maeda, Gribble, et al , 2020) . Likewise, when monkeys generate elbow reaches or respond to perturbations that created pure elbow motion in our study, shoulder muscle activity begins before movement onset (Figure 2 C-D), and shows a quick shoulder responses within 50-100 ms post perturbation (i.e., long-latency epoch; Figure 3 C-D), respectively.…”

“…One complexity of such movements are the mechanical interactions that arise across moving limb segments, as movements around one joint cause rotational forces at other joints (Hollerbach & Flash, 1982;Graham et al , 2003) . Many previous studies have demonstrated that the nervous system develops an internal representation of such arm dynamics that can be used to generate predictive (i.e., feedforward) muscle activity during self-initiated reaching (Gribble & Ostry, 1999;Debicki & Gribble, 2005;Gritsenko et al , 2011;Maeda et al , 2017Maeda et al , , 2018Maeda, Gribble, et al , 2020;Maeda, Zdybal, et al , 2020a, 2020b and also reflex (i.e., feedback) responses to mechanical perturbations, in a way that accounts for the arm dynamics (Lacquaniti & Soechting, 1984, 1986a, 1986bSoechting & Lacquaniti, 1988;Kurtzer, Pruszynski, et al , 2006;Kurtzer et al , 2008Kurtzer et al , , 2009Kurtzer et al , , 2014Kurtzer et al , , 2016Pruszynski et al , 2011;Crevecoeur et al , 2012;Maeda et al , 2017Maeda et al , , 2018Kurtzer, 2019;Maeda, Gribble, et al , 2020) . For instance, when generating single-joint elbow movements and when responding to mechanical perturbations that create pure elbow motion, the nervous system generates predictive shoulder muscle activity and robust shoulder feedback responses to counter the underlying torques that arise at the shoulder joint because of forearm rotation about the elbow joint (Gribble & Ostry, 1999;Kurtzer et al , 2008;Maeda et al , 2017Maeda et al , , 2018Maeda, Gribble, et al , 2020) .…”