Skip to main content
SpringerLink
Log in

The effect of fasciculus cuneatus lesions on finger positioning and long-latency reflexes in monkeys

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Previous studies have reported abnormalities in fine hand and finger movements following interruption of the fasciculus cuneatus (FC) in primates. We report here that many of these deficits could be caused by an inability to actively regulate the position of the finger. Three macaques were trained to maintain the index finger in one position against constant or changing loads. Periodically, torque pulses were used to elicit reflexes in finger muscles. Following unilateral FC lesions, the monkeys failed to adjust finger position during the trials, and the normal M2 long-latency response was absent in the finger muscles. Performance on the task was impaired only in monkeys with complete lesions that included the deep ventral portion of the FC. These results suggest that afferent fibers in the FC regulate finger position, and do so partly through reflexive mechanisms. When the FC is interrupted, the inability to control finger position disturbs fine motor activities.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Asanuma H, Larsen KD, Yumiya H (1979) Direct sensory pathway to the motor cortex: a basis of cortical reflexes. In: Asanuma H, Wilson VJ (eds) Integration in the nervous system. Igaku-shoin, New York, pp 223–238

    Google Scholar 

  • Asanuma H, Larsen KD, Yumiya H (1980) Peripheral input pathways to the monkey motor cortex. Exp Brain Res 38:349–355

    Google Scholar 

  • Basmajian JV, DeLuca CJ (1983) Muscles alive: their functions revealed by electromyography, 5th edn Williams and Wilkins, Baltimore

    Google Scholar 

  • Beck C (1976) Forelimb performance by squirrel monkeys (Saimiri sciureus) before and after dorsal column lesions. J Comp Physiol Psychol 90:353–362

    Google Scholar 

  • Berkley KJ (1980) Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatic sensory inputs to the lateral diencephalon. J Comp Neurol 193:283–317

    Google Scholar 

  • Berkley KJ, Vierck CJ Jr (1987) Transient changes in retrograde labeling of diencephalic-projecting neurons in monkey dorsal collumn nuclei following removal of their dorsal column input. In: Pubols L, Sessle B (eds) Effects of injury on somatosensory systems. Liss, New York, pp 429–436

    Google Scholar 

  • Brinkman J, Bush BM, Porter R (1978) Deficient influences of peripheral stimuli on precentral neurones in monkeys with dorsal column lesions. J Physiol (Lond) 276:27–48

    Google Scholar 

  • Capaday C, Forget R, Fraser R, Lamarre Y (1991) Evidence for a contribution of the motor cortex to the long-latency stretch reflex of the human thumb. J Physiol (Lond) 440:243–255

    Google Scholar 

  • Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44:773–791

    Google Scholar 

  • Cheney PD, Fetz EE (1984) Corticomotoneuronal cells contribute to long-latency stretch reflexes in the Rhesus monkey. J Physiol (Lond) 349:249–272

    Google Scholar 

  • Clark FJ, Burgess RC, Chapin JW, Lipscomb WT (1985) Role of intramuscular receptors in the awareness of limb position. J Neurophysiol 54:1529–1540

    Google Scholar 

  • Clark SA, Allard T, Jenkins WM, Merzenich MM (1988) Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature 332:444–445

    Google Scholar 

  • Cook AW, Browder EJ (1965) Function of the posterior columns in man. Arch Neurol 12:72–79

    Google Scholar 

  • Cooper BY, Kibria KM, Vierck CJ (1986) Exgen: An apple II-based software package for the control of peripheral devices and acquisition of digital and analog data. J Electrophy siol Tech 13:9–19

    Google Scholar 

  • Cooper BY, Schulmann DL, Leonard CM, Vierck CJ (1988) Finger movement disorders following section of the dorsal columns. Soc Neurosci Abstr (USA) 14:954

    Google Scholar 

  • Cooper BY, Glendinning DS, Vierck CJ (1992) Finger movement deficits in the stumptail macaque following lesions of cuneate fasciculus. Somatosensory and Motor Res (in press)

  • Cordo PJ (1990) Kinesthetic control of a multijoint movement sequence. J Neurophysiol 63:161–172

    Google Scholar 

  • Dreyer D, Schneider RJ, Mitz CB, Whitsel BL (1974) Differential contributions of spinal pathways to body representation in postcentral gyrus of Macaco mulatta. J Neurophysiol 37:119–145

    Google Scholar 

  • Dykes RW, Rasmusson DD, Stretavan D, Rehman NB (1982) Submodality segregation and receptive-field sequences in cuneate, gracile, and external cuneate nuclei of the cat. J Neurophysiol 47:389–416

    Google Scholar 

  • Evarts EV (1973) Motor cortex reflexes associated with learned movement. Science 179:501–503

    Google Scholar 

  • Evarts EV (1985) Sherrington's concept of proprioception. In: Evarts EV, Wise SP, Bousfield D (ed) The motor system in neurobiology. Elsevier, New York, pp 183–186

    Google Scholar 

  • Evarts EV, Tanji J (1976) Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. J Neurophysiol 39:1069–1080

    Google Scholar 

  • Ferraro A, Barrera SE (1934) Effects of experimental lesions of the posterior columns in Macacus Rhesus monkeys. Brain 57:307–332

    Google Scholar 

  • Ferrell WR, Smith A (1987) The effect of digital nerve block on position sense at the proximal interphalangeal joint of the human index finger. Brain Res 425:369–371

    Google Scholar 

  • Fetz EE, Finocchio DV, Baker MA, Soso MJ (1980) Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. J Neurophysiol 43:1070–1110

    Google Scholar 

  • Forget R, Lamarre Y (1987) Rapid elbow flexion in the absence of proprioceptive and cutaneous feedback. Hum Neurobiol 6:27–37

    Google Scholar 

  • Fromm C, Evarts EV (1978) Motor cortex responses to kinesthetic inputs during postural stability, precise fine movement and ballistic movement in the conscious monkey. In Gordon G (ed) Active touch. Pergamon, New York, pp 105–118

    Google Scholar 

  • Fyffe REW, Cheema SS, Rustioni A (1986) Intracellular staining study of the feline cuneate nucleus. I. Terminal patterns of primary afferent fibers. J Neurophysiol 56:1268–1282

    Google Scholar 

  • Gandevia SC, McCloskey DI (1976) Joint sense, muscle sense, and their combination as position sense, measured at the distal interphalangeal joint of the middle finger. J Physiol (Lond) 206:387–407

    Google Scholar 

  • Gandevia SC, McCloskey DI (1977) Effects of related sensory inputs on motor performances in man studied through changes in perceived heaviness. J Physiol (Lond) 272:653–672

    Google Scholar 

  • Ghez C, Shinoda Y (1978) Spinal mechanisms of the functional stretch reflex. Exp Brain Res 32:55–68

    CAS  PubMed  Google Scholar 

  • Gilman S, Denny-Brown D (1966) Disorders of movement and behaviour following dorsal column lesions. Brain 89:397–417

    Google Scholar 

  • Glendinning DS (1991) Fine motor control deficits in monkeys following dorsal column lesions (doctoral dissertation). University of Florida, Gainesville

    Google Scholar 

  • Glendinning DS, Vierck CJ Jr (1991) Effects of dorsal column lesions on motor control and long-latency responses in the index finger of macaques. Soc Neurosci Abstr (USA) 17:1223

    Google Scholar 

  • Glendinning DS, Cooper BY, Vierck CJ Jr, Leonard CM (1992) Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions. Somatosens Mot Res 9:61–73

    Google Scholar 

  • Glendinning DS, Vierck CJ Jr (1992) Lack of proprioceptive deficit after dorsal column lesions in monkeys. Neurology (in press)

  • Hammond PH (1955) Involuntary activity in biceps following the sudden application of velocity to the abducted forearm. J Physiol (Lond) 127:23–25

    Google Scholar 

  • Hirai T, Jones EG (1988) Segregation of lemniscal inputs and motor cortex outputs in cat ventral thalamic nuclei: application of a novel technique. Exp Brain Res 71:329–344

    Google Scholar 

  • Hongo T, Kitazawa S, Ohki Y, Sasaki M, Xi M (1989a) A physiological and morphological study of premotor interneurones in the cutaneous reflex pathways in cats. Brain Res 505:163–166

    Google Scholar 

  • Hongo T. Kitazawa S, Ohki Y, Xi M (1989b) Functional identification of last-order interneurones of skin reflex pathways in the cat forelimb segments. Brain Res 505:167–170

    Google Scholar 

  • Jenner JR, Stephens JA (1982) Cutaneous reflex responses and their central nervous system pathways studied in man. J Physiol (Lond) 333:405–419

    Google Scholar 

  • Johansson RS, Westling G (1987) Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp Brain Res 66:141–154

    CAS  PubMed  Google Scholar 

  • Jones EG (1983) The nature of the afferent pathways conveying short-latency inputs to primate motor cortex. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven, New York, pp 263–285

    Google Scholar 

  • Jones EG (1984) Organization of the thalamocortical complex and its relation to sensory processes. In: Darian-Smith I (ed) Handbook of Physiology, Section 1: The nervous system, vol III, Sensory processes, part 1. American Physiological Society, Bethesda, pp 149–212

    Google Scholar 

  • Kanda K, Desmedt JE (1983) Cutaneous facilitation of large motor units and motor control of human fingers in precision grip. In Desmedt JE (ed) Motor control mechanisms in health and disease. Raven Press, New York, pp 253–262

    Google Scholar 

  • Kendall FP, McCreary EK (1983) Muscles, testing and function, 3rd edn, Williams and Wilkins, Baltimore

    Google Scholar 

  • Lawrence DG, Kuypers HGJM (1968) The functional organization of the motor system in the monkey I. The effects of bilateral pyramidal lesions. Brain 91:1–13

    Google Scholar 

  • Lee RG, Tatton WG (1975) Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Can J Neurol Sci 2:285–293

    CAS  Google Scholar 

  • Leonard CM, Glendinning DS, Wilfong T, Cooper BY, Vierck CJ (1992) Alterations of natural hand movements after interruption of fasciculus cuneatus in the macaque. Somatosens Mot Res 9:75–89

    Google Scholar 

  • Marsden CD, Merton PA, and Morton HB (1973) Latency measurements compatible with a cortical pathway for the stretch reflex in man. J Physiol (Lond) 230:58–59

    Google Scholar 

  • Marsden CD, Merton PA, Morton HB (1977a) The sensory mechanism of servo action in human muscle. J Physiol (Lond) 265:521–535

    Google Scholar 

  • Marsden CD, Merton PA, Morton HB, Adam J (1977b) The effect of posterior column lesions on servo responses from the human long thumb flexor. Brain 100:185–200

    Google Scholar 

  • Marsden CD, Rothwell JC, Day BL (1983) Long-latency automatic responses to muscle stretch in man: origin and function. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven Press, New York, pp 509–540

    Google Scholar 

  • Mathews PBC (1989) Long-latency stretch reflexes of two intrinsic muscles of the human hand analysed by cooling the arm. J Physiol (Lond) 419:519–538

    CAS  PubMed  Google Scholar 

  • Mathews PBC (1991) The human stretch reflex and the motor cortex. Trends Neurosci 14:87–91

    Google Scholar 

  • McCloskey D, Ebeling P, and Goodwin GM (1974) Estimation of weights and tensions and apparent involvement of a ‘sense of effort’. Exp Neurol 42:220–232

    Google Scholar 

  • Miller, AD, Brooks VB (1981) Late muscular responses to arm perturbations persist during supraspinal dysfunctions in monkeys. Exp Brain Res 41:146–158

    Google Scholar 

  • Nathan PW, Smith MC, Cook AW (1986) Sensory effects in man of lesions of the posterior columns and of some other afferent pathways. Brain 109:1003–1041

    Google Scholar 

  • Phillips CG (1969) Motor apparatus of the baboon's hand. Proc Roy Soc B 173:141–174

    Google Scholar 

  • Rafferty J, Norling R, McMath C, Tamarn R, Morganstein D (1985) Statworks. Cricket Software, Philadelphia

    Google Scholar 

  • Ralston HJ III (1991) Local circuitry of the somatosensory thalamus in the processing of sensory information. Prog Brain Res 87:13–28

    Google Scholar 

  • Rosen I, Asanuma H (1972) Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-output relations. Exp Brain Res 14:257–273

    Google Scholar 

  • Sanes JN, Mauritz KH, Dalakas MC, Evarts EV (1985) Motor control in humans with large-fiber sensory neuropathy. Hum Neurobiol 4:101–114

    Google Scholar 

  • Schwartzman RG, Bogdonoff MD (1969) Proprioception and vibration sensibility discrimination in the absence of the posterior columns. Arch Neurol 20:349–353

    Google Scholar 

  • Shriver JE, Stein BM, Carpenter MB (1968) Central projections of spinal dorsal roots in the monkey. I. Cervical and upper thoracic dorsal roots. Am J Anat 123:27–74

    Google Scholar 

  • Strick PL (1976) Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J Neurophysiol 39:1020–1031

    Google Scholar 

  • Strick PL (1978) Cerebellar involvement in ‘volitional’ muscle responses to load changes. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Karger, Basel, pp 85–93

    Google Scholar 

  • Strick PL, Preston JB (1982) Two representations of the hand in area 4 of a primate. I. Motor output organization. J Neurophysiol 48:139–149

    Google Scholar 

  • Tatton WG, Forner SD, Gerstein GL, Chambers WW, Liu CN (1975) The effect of postcentral cortical lesions on motor responses to sudden upper limb displacements in monkeys. Brain Res 96:108–113

    Google Scholar 

  • Tatton WG, Bawa P, Bruce IC, Lee RG (1978) Long loop reflexes in monkeys: an interpretative base for human reflexes. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Karger, Basel, pp 229–245

    Google Scholar 

  • Tower SS (1940) Pyramidal lesion in the monkey. Brain 63:36–90

    Google Scholar 

  • Tracey DJ, Asanuma C, Jones EG, Porter R (1980a) Thalamic relay to motor cortex: afferent pathways from brain stem, cerebellum, and spinal cord in monkeys. J Neurophysiol 44:532–554

    Google Scholar 

  • Tracey DJ, Walmsley B, Brinkman J (1980b) ‘Long-loop’ reflexes can be obtained in spinal monkeys. Neurosci Lett 18:59–65

    Google Scholar 

  • Uddenburg N (1968a) Differential localization in dorsal funiculus of fibres originating from different receptors. Exp Brain Res 4:367–376

    Google Scholar 

  • Uddenburg N (1968b) Functional organization of long, second-order afferents in the dorsal funiculus. Exp Brain Res 4:377–382

    Google Scholar 

  • Vierck CJ Jr (1975) Proprioceptive deficits after dorsal column lesions in monkeys. In: Kornhuber H (ed) The somatosensory system. Thieme, Stuttgart, pp 310–317

    Google Scholar 

  • Vierck CJ Jr (1978a) Comparison of forelimb and hindlimb motoric deficits following dorsal column section in monkeys. Brain Res 146:279–294

    Google Scholar 

  • Vierck CJ Jr (1978b) Interpretations of the sensory and motor consequences of dorsal column lesions. In: Gordon G (ed) Active touch. Pergamon Press, New York, pp 139–158

    Google Scholar 

  • Vierck CJ Jr (1982a) Comparison of the effects of dorsal rhizotomy or dorsal column transection on motor performance of monkeys. Exp Neurol 75:566–575

    Google Scholar 

  • Vierck CJ Jr (1982b) Plasticity of somatic sensations and motor capacities following lesions of the dorsal spinal columns in monkeys. In: Morrison AR, Strick PL (eds) Changing concepts of the nervous system. Academic Press, New York, pp 151–169

    Google Scholar 

  • Vierck CJ Jr (1984) The spinal lemniscal pathways. In: Davidoff RA (ed) Handbook of the spinal cord. Dekker, New York, pp 673–749

    Google Scholar 

  • Vierck CJ Jr, Cooper BY (1990) Epicritic sensations of primates. In: Berkley MA, Stebbins WC (eds) Comparative perception, vol 1, Basic mechanisms. Wiley, New York, pp 29–66

    Google Scholar 

  • Vierck CJ Jr, Cohen RH, Cooper BY (1985) Effects of spinal lesions on temporal resolution of cutaneous sensations. Somatosensory Res 3:45–56

    Google Scholar 

  • Vierck CJ Jr, Cooper BY, Leonard CM (1987) Motor capacities and deficiencies after interruption of the dorsal spinal columns in primates. In: Pubols L, Sessle B (eds) Effects of injury on trigeminal and spinal somatosensory systems. (Neurology and Neurobiology, vol 30) Liss, pp 419–427

  • Vierck CJ Jr, Whitsel BL, Kulics AT, Cooper BY (1990) Alterations of a cortical network of neurons following interruption of the dorsal spinal columns. In: Seil F (ed) Advances in neural regeneration research: proceedings of the third international neural regeneration research symposium. (Neurology and neurobiology, vol 60) Wiley-Liss, New York, pp 335–368

    Google Scholar 

  • Walker AE, Weaver TA (1942) The topical organization and termination of the fibers of the posterior columns in Macaco mulatta. J Comp Neurol 76:145–158

    Google Scholar 

  • Wall PD (1970) The sensory and motor role of impulses travelling in the dorsal columns toward cerebral cortex. Brain 93:505–524

    Google Scholar 

  • Waters RS, Tamai Y, Asanuma H (1985) Caudal cuneate nucleus projection of the direct thalamic relay to the motor cortex: an electrophysiological study. Brain Res 360:361–365

    Google Scholar 

  • Watson JDG, Colebatch JG, McCloskey DI (1984) Effects of externally imposed elastic loads on the ability to estimate position and force. Behav Brain Res 13:267–271

    Google Scholar 

  • Wise SP, Tanji J (1981) Supplementary and percentral motor cortex. Contrast in responsiveness to peripheral input in the hindlimb area of the unanaesthetized monkey. J Comp Neurol 195:433–451

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience and Center for Neurobiological Sciences, University of Florida Colleges of Medicine and Dentistry, 32610, Gainesville, FL, USA

    Diana S. Glendinning & Charles J. Vierck Jr.

  2. Department of Oral and Maxillofacial Surgery, University of Florida Colleges of Medicine and Dentistry, 32610, Gainesville, FL, USA

    Brian Y. Cooper

Authors
  1. Diana S. Glendinning
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles J. Vierck Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian Y. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Glendinning, D.S., Vierck, C.J. & Cooper, B.Y. The effect of fasciculus cuneatus lesions on finger positioning and long-latency reflexes in monkeys. Exp Brain Res 93, 104–116 (1993). https://doi.org/10.1007/BF00227785

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227785

Key words

Search

Navigation