APAs Constraints to Voluntary Movements: The Case for Limb Movements Coupling

Abstract

When rhythmically moving two limbs in either the same or in opposite directions, one coupling mode meets constraints that are absent in the other mode. Isodirectional (ISO) flexion-extensions of the ipsilateral hand and foot can be easily performed with either the hand prone or supine. Instead, antidirectional (ANTI) movements require attentive effort and irresistibly tend to reverse into ISO when frequency increases. Experimental evidence indicates that the direction dependent easy-difficult dichotomy is caused by interference of the anticipatory postural commands associated to movements of one limb with voluntary commands to the other limb. Excitability of the resting wrist muscles is subliminally modulated at the period of ipsilateral foot oscillations, being phase-opposite in the antagonists and distributed so as to facilitate ISO and obstacle ANTI coupling of the hand (either prone or supine) with the foot. Modulation is driven by cortical signals dispatched to the forearm simultaneously with the voluntary commands moving the foot. If right foot oscillations are performed when standing on the left foot with the right hand touching a fixed support, the subliminal excitability modulation is replaced by overt contractions of forearm muscles conforming the APAs features. This suggests that during hand-foot ANTI coupling the voluntary commands to forearm muscles are contrasted by APAs commands of opposite sign linked to foot oscillations. Correlation between the easy-difficult dichotomy and the APAs distribution is also found in coupled adduction-abduction of the arms or hands in the transverse plane and in coupled flexion-extension of the arms in the parasagittal plane. In all these movements, APAs commands linked to the movement of each limb reach the motor pathways to the contralateral muscles homologous to the prime movers and can interfere during coupling with their voluntary activation. APAs are also generated in postural muscles of trunk and lower limbs and size-increase when the movement frequency is incremented. The related increase in postural effort apparently contributes in destabilizing the difficult coupling mode. Motor learning may rely upon more effective APAs. APAs and focal contraction are entangled within the same voluntary action. Yet, neural diseases may selectively impair APAs, which represent a potential target for rehabilitation.

Keywords: APAs; APAs destabilizing effects on coupling; coupled movements synchronization; direction principle; in phase and antiphase coupling; limb movements coupling; motor learning/training.

Figure 1

The “direction principle” in hand-foot coupling. (A) Subjects seated on an armchair, with the forearms supported in horizontal position, either prone, or supine. The right hand and foot were fixed to basculating supports, free to cover full-range flexion-extensions of the wrist and ankle. Despite their lower frequency, the ANTIdirectional (difficult) oscillations spontaneously reverse (blue arrow) to the easier ISOdirectional coupling. Time calibration, 1 s. (B,C) Schematic illustration of ISO and ANTI coupling of the arm cyclic movements in the horizontal and parasagittal plane, respectively. Reproduced from Baldissera et al. (1982) © Elsevier 1982, with permission of Elsevier.

Figure 2

(A) the phase difference between the two movements (hand-foot ΔΦ, filled black circles) remains mostly unmodified over the entire frequency range. (B) at 1.2 Hz the upward rotation of the two limbs and the onset of the integrated EMGs in the respective movers ECR, Extensor Carpi Radialis; TA, Tibialis Anterior, all start synchronously. (C) at 3.2 Hz, both movements lag the EMG burst onsets, the hand to a larger extent than the foot (black arrows), revealing that the two limbs have different mechanical features. This difference, however, is compensated for by a calibrated advance of the ECR on the TA burst (ECR-TA ΔΦ, blue arrow) which increases with frequency (open circles in A) and maintains the movements synchronism. Reproduced from Baldissera et al. (2000), © Springer-Verlag Berlin Heidelberg 2000, with permission of Springer.

Figure 3

(A) Cyclic modulation the H-reflex size, phase-opposite in the two forearm antagonists ECR (open circles) and FCR (filled circles), at 5 delays during ipsilateral foot oscillations.Modulation is expressed as the absolute deviation of the reflex size from the cycle mean value and is plotted together with the angular position of the ipsilateral foot (foot mov, dorsal flexion up) and the EMG activity in TA muscle (TA EMG). Best-fit sinusoidal functions (solid lines) with the same period as movement are superimposed to the H-reflex plots. Crossing between the two H modulation sine waves (dashed blue line) occurs almost synchronously with both the foot flexion peak (open arrowhead) and the onset of TA activation (filled arrowhead). After foot inertial loading (B) the foot flexion peak lags the onset of the TA burst by about 90°, while the H-reflex modulation remains phase-linked to the TA activation, showing to be insensitive to the afferent signals monitoring the phase shift of the foot position. Figure assembled with data from Cerri et al. (2003) and Borroni et al. (2004).

Figure 4

Frequency dependent changes of the clock-mov phase-delay during separate oscillations of the hand and foot (green dashed and continuous lines, respectively) and during hand-foot ISO coupling (hand, blue circles; foot, red triangles). (A) When both limbs are unloaded the clk-mov delay of each limb, no matter whether isolated or coupled, remains nearly constant over the whole frequency range. (B) same relations as in (A) but obtained after applying an inertial load to the hand. Loading induced the expected increase of the hand clk-mov delay as the frequency is raised but in either limb the frequency relations obtained during separate and coupled movements still superimpose. Reproduced from Baldissera et al. (2006), © 2006 Baldissera et al; licensee BioMed Central Ltd.

Figure 5

When standing on the left foot, with the right hand touching a fixed support (inset), cyclic oscillations of right foot modulate sinusoidally the EMG activity of ipsilateral wrist muscles at the frequency of the foot movement (1.5 Hz). Soleus (SOL) EMG reversed. (A) hand prone, palmar contact; FCR EMG is cyclically modulated, the positive phase coincides with SOL activation. (B) dorsal contact; the positive phase of the ECR EMG modulation coincides with TA activation. (C,D) hand supination reverses the above pattern. In this and the following figures the white lines superimposed to the EMG recordings are the best fit sine-waves with the same period as the movements. Reproduced from Baldissera and Esposti (2005) © Wolters Kluwer Health, Inc. 2005, with permission of Wolters Kluwer Health, Inc.

Figure 6

(A) Hand prone, dorsal contact. Red traces: TA contraction and the ensuing foot dorsal flexion are preceded by an excitatory APA in ECR, the “isodirectional” mover of the hand. Black traces: contraction of SOL and foot plantar flexion are preceded by an inhibitory APA in ECR. (B) Hand supine, dorsal contact. Red traces: an excitatory APA in ECR precedes contraction of the “isodirectional” SOL and foot plantar flexion. Black traces: when the movement direction is inverted to dorsal, ECR becomes “antidirectional” to SOL and the APA changes to inhibitory. Reproduced from Baldissera and Esposti (2005) © Wolters Kluwer Health, Inc. 2005, with permission of Wolters Kluwer Health, Inc.

Figure 7

(A) Contraction of the right rPM in the absence of any fixation chain would counter-rotate the right arm and the trunk. A pure arm movement is obtained if the trunk rotation is opposed by APAs in the fixation chain between the arms (B) and/or to the ground (C). (D) Fast adduction of the right arm in the horizontal plane, prime mover right rPM. Subject sitting on a turnable chair, palmar surface of the left hand touching a fixed support. Excitatory APAs develop in left arm muscles lPM and lFCR, inhibitory APAs in lIS. All APAs precede the prime mover contraction (dashed line). No inhibition is seen in lECR, due to the absence of any background activity. (E) Activation of the rPM is preceded by excitatory APAs in both the lPM and the rIC, while lIC is simultaneously inhibited. The related change of Tz starts simultaneously with the rPM activation. cw, clock-wise. Reproduced from Baldissera et al. (2008a,b), © Springer-Verlag Berlin Heidelberg 2008, with permission of Springer.

Figure 8

Cyclic postural adjustments during rhythmic oscillations in the horizontal plane of the right arm alone (A) and of both arms in ANTI and ISO coupling (B,C). Prime movers, rPM in (A), rPM and lPM in (B,C). During one arm movements, cyclic APAs develop both in lPM and, phase-opposite, in rIC and lIC. This same pattern of EMG modulation, but doubled in size, is present in IC muscles during ISO (difficult) coupling (C). During ANTI coupling, instead, activity is absent in lIC and minimal in rIC (B). In all coupling modes, Tz undergoes changes parallel to the IC activities; cw, clock-wise. Reproduced from Baldissera et al. (2008b), © Springer-Verlag Berlin Heidelberg 2008, with permission of Springer.

Figure 9

(A) Voluntary activation of rAD and acceleration (r arm acc) of the ensuing arm flexion. Vertical dashed line: onset of the rAD EMG burst. (B) APAs in the left arm muscles, excitatory in lAD and lLD and inhibitory in lPD. (C) excitatory APAs in trunk muscles rES and lES and in the right leg muscle rIC. (D) anterior-posterior force Fy and clockwise moment about the body vertical axis Tz, discharged to the ground. (E). Fy and Tz changes are displayed on a longer time base. Dashed line: onset of prime mover burst; cw, clock-wise. Reproduced from Esposti and Baldissera (2013), © Springer-Verlag Berlin Heidelberg 2013, with permission of Springer.

Figure 10

Voluntary oscillations of both arms in the parasagittal plane. ISO and ANTI coupling. Same labels as in Figure 9. (A,D): cyclic voluntary EMG activity in rAD and lAD muscles and ensuing oscillations of the right and left arms. In ISO coupling the activation of both trunk (ES) and thigh (IC) postural muscles is synchronous on the two sides (B) and corresponds (C) to a clear-cut anterior-posterior ground reaction Fy while the torque Tz is marginal. (E) in ANTI coupling, the EMG modulation in rES and lES remains synchronous but consistently lower with respect to ISO, whereas the IC activation is increased in size and is phase-opposite in rIC and lIC. Correspondingly (F), a large reaction torque Tz is generated while Fy is strongly reduced. Reproduced from Baldissera and Esposti (2013), © Springer-Verlag Berlin Heidelberg 2013, with permission of Springer.

Figure 11

Coordination marker SDΔΦ and postural markers Fy and Tz recorded during coupled arm movements performed by the same subjects in both the horizontal and parasagittal planes (red triangles and blue circles, respectively). Filled symbols, stable (easy) modes; open symbols, unstable (difficult) modes. (A) SDΔφ is identical in the easy modes pISO and hANTI, larger in pANTI and even more so in hISO. Small symbols and dashed lines: values obtained in only part of the subjects. (B) Tz is virtually null in the two easy modes (filled symbols) and not significantly different between the two movement types. Instead, it increases with frequency in the two difficult modes (open symbols), more in hISO than in pANTI. Above 2.0–2.4 Hz, Tz starts however to decrease progressively. Size of Fy increases monotonically with frequency up to 3.4 Hz in pISO while it remains negligible in the other three movement combination. Reproduced from Baldissera and Esposti (2013), © Springer-Verlag Berlin Heidelberg 2013, with permission of Springer.

Figure 12

Relations of the oscillation frequency with the normalized oxygen uptake Δ$\dot{\text{V}}$O₂ (A) as well as with the coupling variability SDΔΦ (B), in either coupling mode of the horizontal and parasagittal movements (black and blue symbols, respectively). In (C), direct correlation between SDΔΦ and Δ$\dot{\text{V}}$O₂. The SDΔΦ-Δ$\dot{\text{V}}$O₂ relation in the two difficult modes (pANTI and hISO) runs higher and has a higher slope than in the respective easy modes (pISO and hANTI). Continuous arrow in (B): total ISO-vs.-ANTI stability loss; dashed arrow in (C): stability loss independent from Δ$\dot{\text{V}}$O₂. Both are marked at 2.6 Hz. In (D) the total and the non-metabolic stability losses in parasagittal movements are plotted by a continuous and dashed lines, respectively, so as to separate the two components of the stability loss, namely the neural conflict and the postural effort. Reproduced from Esposti et al. (2013), © Springer-Verlag Berlin Heidelberg 2013, with permission of Springer.

Figure 13

A cerebellar patient (left panel) is requested to lean backward (focal movement) while standing. If not supported by the assistant, he will fall. The right panel shows the correct movement, in which knee flexion (APA) precedes the trunk extension, so that the body center of mass will be projected within the base of support (“cerebellar asynergy,” after Babinski, 1899). This established clinical finding was confirmed by later, refined neurophysiologic research. Yet, after nearly 120 years this still remains one of the brightest demonstrations that the postural component of a voluntary moment can be impaired independently from its focal component.