Skip to main content

Advertisement

Log in

Hierarchical control of static prehension: I. Biomechanics

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We explored the action of digits during static prehension tasks involving one hand or two hands of one or two persons. Three hypotheses were tested: to prevent slippage of the object, grip force and safety margin (SM) would be largest in bimanual conditions, particularly involving two persons; the distribution of tangential forces would not differ among tested conditions, thus preserving the vertical orientation of the object in a stereotypical way; and the mechanical advantage of fingers would be used to maintain rotational equilibrium. The multi-digit synergies are discussed in the companion paper (Gorniak et al. 2009, in review). The subjects held vertical one of the two handles, a narrow one and a wide one. They used the four fingers of the right hand opposed by either the right hand thumb, the left hand thumb, the left hand index finger, the thumb of an experimenter, the index finger of an experimenter, or an inanimate object. Forces and moments of force produced by each digit were recorded. The first two hypotheses were falsified. Both grip force and SM were the largest in the one-hand task, and they were the lowest for the tasks involving two persons. The distribution of tangential forces among fingers was significantly different in the one-hand task. The mechanical advantage hypothesis was supported across all the tested conditions. The results suggest that the neural controller uses a different strategy in the one-hand task as compared to other tasks, while bimanual prehension involving two persons differs from one-person two-hand tasks. The findings do not support a hypothesis that normal (grip) forces are adjusted to ensure a particular value of the SM. Maintaining rotational equilibrium was achieved differently in different tasks. In particular, the one-hand task was characterized by large intercompensated adjustments in different contributors to the total moment of force, which could be described as chain effects; such adjustments were all but absent in the other conditions. The findings may be interpreted within the framework of the reference configuration hypothesis, in which digit forces emerge due to the discrepancies between the actual and the centrally defined (reference) hand aperture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. Exp Brain Res Suppl 10:111–129

    Google Scholar 

  • Bernstein NA (1996) On dexterity and its development. In: Latash ML, Turvey MT (eds) dexterity and its development. Erlbaum, Mahwah

    Google Scholar 

  • Boudreau MJ, Smith AM (2001) Activity in rostral motor cortex in response to predictable force-pulse perturbations in a precision grip task. J Neurophysiol 86:1079–1085

    PubMed  CAS  Google Scholar 

  • Burstedt MK, Edin BB, Johansson RS (1997) Coordination of fingertip forces during human manipulation can emerge from independent neural networks controlling each engaged digit. Exp Brain Res 117:67–79

    Article  PubMed  CAS  Google Scholar 

  • Burstedt MK, Flanagan JR, Johansson RS (1999) Control of grasp stability in humans under different frictional conditions during multidigit manipulation. J Neurophysiol 82:2393–2405

    PubMed  CAS  Google Scholar 

  • Cesari P, Newell KM (1999) The scaling of human grip configurations. J Exp Psych Hum Percept Perf 25:927–935

    Article  CAS  Google Scholar 

  • Cesari P, Newell KM (2000) Body-scaled transitions in human grip configurations. J Exp Psych: Hum Percept Perf 26:1657–1668

    Article  CAS  Google Scholar 

  • Cole KJ, Rotella DL, Harper JG (1999) Mechanisms for age-related changes of fingertip forces during precision gripping and lifting in adults. J Neurosci 19:2338–3247

    Google Scholar 

  • Davidson PR, Wolpert DM (2005) Widespread access to predictive models in the motor system: a short review. J Neural Eng 2:S313–S319

    Article  PubMed  Google Scholar 

  • Feldman AG (1966) Functional tuning of the nervous system with control of movement or maintenance of a steady posture–II. Controllable parameters of the muscles. Biophysics 11:565–578

    Google Scholar 

  • Feldman AG (1986) Once more on the equilibrium point hypothesis (λ model) for motor control. J Mot Behav 18:17–54

    PubMed  CAS  Google Scholar 

  • Feldman AG, Latash ML (2005) Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium point hypothesis. Exp Brain Res 161:91–103

    Article  PubMed  Google Scholar 

  • Feldman AG, Levin MF (1995) Positional frames of reference in motor control: their origin and use. Behav Brain Sci 18:723–806

    Article  Google Scholar 

  • Feldman AG, Ostry DJ, Levin MF, Gribble PL, Mitnitski AB (1998) Recent tests of the equilibrium-point hypothesis (λ model). Motor Control 2:189–205

    PubMed  CAS  Google Scholar 

  • Feldman AG, Goussev V, Sangole A, Levin MF (2007) Threshold position control and the principle of minimal interaction in motor actions. Prog Brain Res 165:267–281

    Article  PubMed  Google Scholar 

  • Flanagan JR, Tresilian JR (1994) Grip-load force coupling: a general control strategy for transporting objects. J Exp Psychol Hum Percept Perform 20:944–957

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JR, Wing AM (1993) Modulation of grasp force with load force during point-to-point arm movements. Exp Brain Res 95:131–143

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JR, Wing AM (1995) The stability of precision grasp forces during cyclic arm movements with a hand-held load. Exp Brain Res 105:455–464

    PubMed  CAS  Google Scholar 

  • Flanagan JR, Wing AM (1997) The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci 17:1519–1528

    PubMed  CAS  Google Scholar 

  • Gao F, Latash ML, Zatsiorsky VM (2005) Internal forces during object manipulation. Exp Brain Res 165:69–83

    Article  PubMed  Google Scholar 

  • Gao F, Latash ML, Zatsiorsky VM (2006) Maintaining rotational equilibrium during object manipulation: linear behavior of a highly non-linear system. Exp Brain Res 169:519–531

    Article  PubMed  Google Scholar 

  • Goodman SR, Latash ML (2006) Feed-forward control of a redundant motor system. Biol Cybern 95:271–280

    Article  PubMed  Google Scholar 

  • Gorniak SL, Zatsiorsky VM, Latash ML (2007a) Hierarchies of synergies: an example of two-hand multi-finger tasks. Exp Brain Res 179:167–180

    Article  PubMed  Google Scholar 

  • Gorniak SL, Zatsiorsky VM, Latash ML (2007b) Emerging and disappearing synergies in a hierarchially controlled system. Exp Brain Res 183:259–270

    Article  PubMed  Google Scholar 

  • Gorniak SL, Duarte M, Latash ML (2008) Do synergies improve accuracy? A study of speed-accuracy trade-offs during finger force production. Motor Control 12:151–172

    PubMed  Google Scholar 

  • Gorniak SL, Zatsiorsky VM, Latash ML (2009) Hierarchical control of static prehension II. Multi-digit synergies. (in review, the companion paper)

  • Hermsdörfer J, Hagl E, Nowak DA, Marquardt C (2003) Grip force control during object manipulation in cerebral stroke. Clin Neurophysiol 114:915–929

    Article  PubMed  Google Scholar 

  • Jenmalm P, Goodwin AW, Johansson RS (1998) Control of grasp stability when humans lift objects with different surface curvatures. J Neurophysiol 79:1643–1652

    PubMed  CAS  Google Scholar 

  • Johansson RS (1996) Sensory control of dextrous manipulation in humans. In: Wing A, Haggard P, Flanagan R (eds) Hand and Brain. Academic Press, San Diego, pp 381–414

    Chapter  Google Scholar 

  • Johansson RS (1998) Sensory input and control of grip. Novartis Foundation Symposia 218:45–59 (discussion 59–63)

    Article  CAS  Google Scholar 

  • Johansson RS (2002) Dynamic use of tactile afferent signals in control of dexterous manipulation. Adv Exp Med Biol 508:397–410

    PubMed  Google Scholar 

  • Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564

    Article  PubMed  CAS  Google Scholar 

  • Johansson RS, Westling G (1987) Significance of cutaneous input for precise hand movements. Electroencephalog Clin Neurophysiol Suppl l 39:53–57

    CAS  Google Scholar 

  • Kinoshita H, Kawai S, Ikuta K, Teraoka T (1996) Individual finger forces acting on a grasped object during shaking actions. Ergonomics 39:243–256

    Article  PubMed  CAS  Google Scholar 

  • Latash ML, Scholz JP, Schoener G (2002) Motor control strategies revealed in the structure of motor variability. Exerc Sport Sci Rev 30:26–31

    Article  PubMed  Google Scholar 

  • Latash ML, Scholz JP, Schoener G (2007) Toward a new theory of motor synergies. Motor Control 11:276–308

    PubMed  Google Scholar 

  • MacKenzie CL, Iberall T (1994) The grasping hand. North Holland (Elsevier Science), Amsterdam

    Google Scholar 

  • Marwaha R, Hall SJ, Knight CA, Jaric S (2006) Load and grip force coordination in static bimanual manipulation tasks in multiple sclerosis. Motor Control 10:160–177

    PubMed  Google Scholar 

  • Matthews PBC (1959) The dependence of tension upon extension in the stretch reflex of the soleus of the decerebrate cat. J Physiol 47:521–546

    Google Scholar 

  • Newell KM, Carlton LG (1993) Force variability in isometric responses. J Exp Psychol Hum Percept Perform 14:37–44

    Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Ostry DJ, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288

    Article  PubMed  Google Scholar 

  • Pataky TC, Latash ML, Zatsiorsky VM (2004) Prehension synergies during nonvertical grasping, I: experimental observations. Biol Cybern 91:148–158

    PubMed  Google Scholar 

  • Pilon J-F, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67

    Article  PubMed  Google Scholar 

  • Reinkensmeyer DJ, Lum PS, Lehman SL (1992) Human control of a simple two-hand grasp. Biol Cybern 67:553–564

    Article  PubMed  CAS  Google Scholar 

  • Shapkova EY, Shapkova AL, Goodman SR, Zatsiorsky VM, Latash ML (2008) Do synergies decrease force variability? A study of single-finger and multi-finger force production. Exp Brain Res 188:411–425

    Article  PubMed  Google Scholar 

  • Shim JK, Latash ML, Zatsiorsky VM (2003) Prehension synergies: trial-to-trial variability and hierarchical organization of stable performance. Exp Brain Res 152:173–184

    Article  PubMed  Google Scholar 

  • Shim JK, Latash ML, Zatsiorsky VM (2004a) Finger coordination during moment production on a mechanically fixed object. Exp Brain Res 157:457–467

    Article  PubMed  Google Scholar 

  • Shim JK, Lay B, Zatsiorsky VM, Latash ML (2004b) Age-related changes in finger coordination in static prehension tasks. J Appl Physiol 97:213–224

    Article  PubMed  Google Scholar 

  • Shim JK, Latash ML, Zatsiorsky VM (2005) Prehension synergies in three dimensions. J Neurophysiol 93:766–776

    Article  PubMed  Google Scholar 

  • Smits-Engelsman BCM, Van Galen GP, Duysens J (2004) Force levels in uni- and bimanual isometric tasks affect variability measures differently throughout the lifespan. Motor Control 8:437–449

    PubMed  Google Scholar 

  • Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nature Neurosci 5:1226–1235

    Article  PubMed  CAS  Google Scholar 

  • Westling G, Johansson RS (1984) Factors influencing the force control during precision grip. Exp Brain Res 53:277–284

    Article  PubMed  CAS  Google Scholar 

  • Witney AG, Wolpert DM (2007) The effect of externally generated loading on predictive grip force modulation. Neurosci Lett 414:10–15

    Article  PubMed  CAS  Google Scholar 

  • Yang JF, Scholz JP, Latash ML (2007) The role of kinematic redundancy in adaptation of reaching. Exp Brain Res 176:54–69

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM (2002) Kinetics of Human Motion. Human Kinetics, Champaign, IL, p 45

    Google Scholar 

  • Zatsiorsky VM, Gregory RW, Latash ML (2002) Force and torque production in static multifinger prehension: biomechanics and control. I. Biomechanics. Biol Cybern 87:50–57

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Gao F, Latash ML (2003a) Finger force vectors in multi-finger prehension. J Biomech 36:1745–1749

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Gao F, Latash ML (2003b) Prehension synergies: effects of object geometry and prescribed torques. Exp Brain Res 148:77–87

    Article  PubMed  CAS  Google Scholar 

  • Zatsiorsky VM, Gao F, Latash ML (2005) Motor control goes beyond physics: differential effects of gravity and inertia on finger forces during manipulation of hand-held objects. Exp Brain Res 162:300–308

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Gao F, Latash ML (2006) Prehension stability: experiments with expanding and contracting handle. J Neurophysiol 95:2513–2529

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Latash ML (2004) Prehension synergies. Exerc Sport Sci Rev 32:75–80

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Latash ML (2008) Prehension synergies: an overview. J Mot Behav 40:446–476

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The study was in part supported by NIH grants AG-018751, NS-035032, and AR-048563. We would like to thank Elizaveta Latash for her assistance in data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark L. Latash.

Appendix

Appendix

In the Appendix, we present the results of analyses that were not crucial for addressing the main hypotheses formulated in “Introduction”. However, we believe that this information may be useful and present it for the sake of completeness.

Normal forces (F n)

Analysis at the IF level

At this level of analysis, normal forces produced by individual fingers of the VF are examined across all tested conditions. Analysis of the individual finger forces within VFR revealed that I R produced larger F n compared to each of the other fingers in VFR across all tested finger configurations and handle widths, as shown in panels a and b of Fig. 4. Panel a shows the contribution of the individual fingers to the F n output of VFR for the narrow handle while panel b shows the contribution of the individual fingers for the wide handle conditions. When fingers of an experimenter were used in the tasks, the smallest values of F n for each of the individual fingers in VFR were produced. Handle width was found to have a significant effect, such that F n(narrow) < F n(wide). These findings were confirmed using ANOVA-1 and ANOVA-2 with the additional factor Finger. Main effects of Width (F 1,351 = 17.15, P < 0.001), Finger Configuration (F 4,351 = 66.69, P < 0.001 and F 5,207 = 86.9, P < 0.001), Finger (F 3,351 = 120.22, P < 0.001 and F 3,207 = 82.23, P < 0.001), and the interaction Finger × Finger Configuration (F 12,351 = 3.69, P < 0.001 and F 12,207 = 6.23, P < 0.001) were found. Pair-wise Tukey tests showed that F n(I R) > F n(MR), F n(RR) > F n(LR). Post hoc analysis also confirmed the finger configurations T E +VFR and I E + VFR having the smallest individual finger values of all tested conditions while the finger configuration T R + VFR yielded the largest individual finger values. The interaction term from ANOVA-1 highlighted the finding that the output of both I R and M R was significantly lower in the T E +VFR and I E + VFR conditions, compared to their output in the T L + VFR, I L + VFR, and Object + VFR conditions. The interaction term from ANOVA-2 revealed that the output for I R, M R, and R R was largest in the configuration T R + VFR compared to all other finger configurations

Moment produced by normal forces (Mn)

Analysis at the VF–TH level

Here we address a question whether the moment of normal forces changed across tested conditions; specifically whether it changed with the number of persons involved in a task. The magnitude of the total moment of normal forces (|M n|) was not affected by any of the tested factors (Finger Configuration or Width) in either ANOVA-1 or ANOVA-2 at the VF–TH level. The M n data averaged across subjects can be found in panel a of Fig. 6

Fig. 6
figure 6

The moment of normal force (M n, a), moment of tangential forces (M t, b), and total moment of force (M TOT, c) are shown for the narrow (white bars) and wide (gray bars) handle widths. The data averaged across all subjects with standard error bars are shown. Abbreviations are the same as in Fig. 2

.

Overall, the magnitude of M n produced by the virtual finger (|M n(VFR)|) changed with the number of persons involved in a given task. In conditions in which digits from an experimenter were used, smaller |M n(VFR)| was produced as compared to all other finger configurations. Panel a of Fig. 7 illustrates that |M n(VFR)| is smallest for tasks involving force production involving two persons for both handle widths where white bars represent the narrow handle data and gray bars represent wide handle data. The data were analyzed using ANOVA-1 and ANOVA-2; a main effect of Finger Configuration (F 4,81 = 6.96, P < 0.001 and F 5,45 = 15.22, P < 0.001) were found. Pair-wise Tukey tests revealed that |M n(VFR)| was largest for the finger configuration T R + VFR and smallest for T E + VFR and I E + VFR.

Fig. 7
figure 7

The moment of normal force (M n, a), moment of tangential forces (M t, b), and total moment of force (M TOT, c) produced by the virtual finger of the right hand are shown for the narrow (white bars) and wide (gray bars) handle widths. The data averaged across all subjects with standard error bars are shown. Abbreviations are the same as in Fig. 2

Moment produced by tangential forces (M t)

Analysis at the VF–TH level

Here, we present the results of analysis of the moment of tangential forces produced by the VF and opposing effector. The magnitude of the total moment of tangential forces (|M t|) was largest when one hand was involved in the task (Object + VFR and T R + VFR) and smallest when both the right and left hands of one person were used (T L + VFR and I L + VFR). Handle width was also found to have significant effects, such that |M t(narrow)| < |M t(wide)|. Data for both the narrow (white bars) and wide handle widths (gray bars) are illustrated in panel b of Fig. 6. Statistical analysis was performed using ANOVA-1 and ANOVA-2; main effects of Width (F 9,81 = 5.22, P < 0.05) and Finger Configuration (F 4,81 = 4.75, P < 0.005 and F 5,45 = 28.23, P < 0.001) were found with no interactions, respectively. Pair-wise post hoc Tukey tests revealed that the magnitude of M t was largest for the T R + VFR and Object + VFR finger configurations but smallest for T L + VFR and I L + VFR.

Further we analyzed how |M t| was shared between the thumb and VF. Analysis of the magnitude of M t produced by the virtual finger (|M t(VFR)|) showed that this value changed with the number of persons involved in a given task. When digits from an experimenter were used, |M t(VFR)| was largest as compared to all other finger configurations. In contrast, when only one hand was involved in the task, |M t(VFR)| was smallest. Width was also determined to be significant, such that |M t(narrow)| < |M t(wide)|. Panel b of Fig. 7 illustrates that |M t(VFR)| is highest for tasks involving force production involving two persons, particularly for the wide handle width. This was confirmed by ANOVA-1 and ANOVA-2, which showed main effects of Width (F 1,81 = 11245.33, P < 0.001) and Finger Configuration (F 4,81 = 17.42, P < 0.001 and F 5,45 = 26.38, P < 0.001) with no interactions. Pair-wise Tukey tests revealed that |M t(VFR)| was the lowest for the Object + VFR and T R + VFR configurations and largest for the T E + VFR and I E + VFR configurations.

Total moment of force (MTOT)

Analysis at the VF–TH level

In this section, the total moment of force produced by the VF and opposing effector is examined across all tested conditions. Overall, the magnitude of total moment of force (|M TOT|) was largest when one hand performed the task (Object + VFR and T R + VFR) compared to all other finger configurations. It was also found that |M TOT | was largest for tasks performed with the narrow handle. The data supporting these claims can be found in panel c of Fig. 6. This was confirmed using ANOVA-1 and ANOVA-2; main effects of Width (F 1,81 = 20.72, P < 0.001) and Finger Configuration (F 4,81 = 14.32, P < 0.001 and F 5,45 = 16.2, P < 0.001) were found with no interactions. Pair-wise Tukey tests revealed that |M TOT | was larger for the narrow handle and for the Object + VFR and T R + VFR conditions as compared to all other finger configurations.

Additional analysis of |M TOT | produced by the virtual finger (|M TOT(VFR)|) was largest when the hands of one person were used in the task (T R + VFR, T L + VFR, and I L + VFR configurations). The data were also affected by handle width, such that |M TOT(narrow)| < |M TOT(wide)|. Panel c of Fig. 7 illustrates that |M TOT(VFR)| was highest for tasks involving hands of the same person, especially for the wide handle width. These findings were confirmed using ANOVA-1; main effects of Width (F 1,81 = 8930.02, P < 0.001), Finger Configuration (F 4,81 = 9.53, P < 0.001 and F 5,45 = 7.24, P < 0.001), and the interaction Width × Finger Configuration (F 4,81 = 5.27, P < 0.005) were found. Pair-wise Tukey tests revealed that |M TOT(VFR)| was the highest for the T R + VFR, T L + VFR, and I L + VFR configurations. The Width × Finger Configuration interaction from ANOVA-1 reflected higher |M TOT(VFR)| in the conditions T L + VFR and I L + VFR compared to I E + VFR and Object + VFR, particularly for the wide handle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gorniak, S.L., Zatsiorsky, V.M. & Latash, M.L. Hierarchical control of static prehension: I. Biomechanics. Exp Brain Res 193, 615–631 (2009). https://doi.org/10.1007/s00221-008-1662-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-008-1662-8

Keywords

Navigation