Summary
The relationship between single cell activity in the “motor” thalamus and the generation of isometric force between the fingers has been investigated in 2 monkeys. Neurons related to the task were found in the thalamic motor regions VLo, VPLo, and VA where microstimulation occasionally elicited motor reactions in hand and fingers. 58% of these 55 neurons, designated “typical”, showed modulation of their discharge patterns with force similar to neurons in precentral cortex and could be assigned to one of 5 discharge patterns described for the motor cortex. Only a small percentage of the thalamic neurons were found to have phasic activity. The other “atypical” neurons (42%) had discharge patterns with complex sequences of phasic and tonic activation with respect to force. For 18 typical and atypical neurons with tonic and phasic-tonic modulation of their firing rate with force significant regression coefficients between firing rate and static force were observed. The mean index of force sensitivity (rateforce slope) was 54.5 Hz/N for the neurons increasing their discharge rate with force, i.e. approximately that of precentral cells. Neurons tested for their sensory properties had receptive fields located on hand and/or fingers and were activated mainly by stimulation of muscle and joint receptors.
The characteristics of these thalamic neurons are compared to those of precentral cells recorded under identical experimental conditions and are discussed in relation to the known input-output relationships of the motor thalamic nuclei. The data strongly support the hypothesis that parameters of movement, in particular force, are represented by the activity of neurons in the “motor” thalamus.
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References
Akert K, Hartmann-von Monakow K (1980) Relationships of precentral, premotor and prefrontal cortex to the mediodorsal and intralaminar nuclei of the monkey thalamus. Acta Neurobiol Exp 40: 7–25
Allum JHJ, Hepp-Reymond M-C, Gysin R (1982) Cross-correlation analysis of interneuronal connectivity in the motor cortex of the monkey. Brain Res 231: 325–334
Allum JHJ, Anner-Baratti REC, Hepp-Reymond M-C (1983) Activity of neurones in the ‘motor’ thalamus and globus pallidus during the control of isometric finger force in the monkey. In: Massion J, Paillard J, Schultz W, Wiesendanger M (eds) Neural coding of motor performance. Exp Brain Res Suppl 7: 194–203
Asanuma C, Thach WT, Jones EG (1983) Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res Rev 5: 237–265
Asanuma H, Fernandez J, Scheibel ME, Scheibel AB (1974) Characteristics of projections from the nucleus ventralis lateralis to the motor cortex in the cats. An anatomical and physiological study. Exp Brain Res 20: 315–330
Carpenter MB (1967) Ventral tier thalamic nuclei. In: Williams D (ed) Modern trends in neurology, Vol 4. Butterworths, London, pp 1–20
Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44: 773–791
Crowell RM, Perret E, Siegfried J, Villoz JP (1968) Movement units and tremor phasic units in the human thalamus. Brain Res 11: 481–488
Deschénes M, Labelle A, Landry P (1979) A comparative study of ventrolateral and recurrent excitatory postsynaptic potentials in large pyramidal tract cells in the cat. Brain Res 160: 37–46
DeVito JL, Anderson ME (1982) An autoradiographic study of efferent connections of the globus pallidus in Macaca mulatta. Exp Brain Res 46: 107–117
Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movements. J Neurophysiol 31: 14–27
Evarts EV (1971) Activity of thalamic and cortical neurons in relation to learned movement in the monkey. Int J Neurol 8: 321–326
Evarts EV, Fromm C, Kröller J, Jennings A (1983) Motor cortex control of finely graded forces. J Neurophysiol 49: 1199–1215
Evarts EV, Kimura M, Wurtz RH, Hikosaka O (1984) Behavioral correlates of activity in basal ganglia neurons. TINS 7: 447–453
Friedman DP, Jones EG (1981) Thalamic input to areas 3a and 2 in monkeys. J Neurophysiol 45: 59–85
Hepp-Reymond M-C, Wyss UR, Anner R (1978) Neuronal coding of static force in the primate motor cortex. J Physiol (Paris) 74: 287–291
Hepp-Reymond M-C, Diener R (1983) Neural coding of force and of rate of force change in the precentral finger region of the monkey. In: Massion J, Paillard J, Schultz W, Wiesendanger M (eds) Neural coding of motor performance. Exp Brain Res Suppl 7: 315–326
Horne MK, Tracey DJ (1979) The afferents and projections of the ventroposterolateral thalamus in the monkey. Exp Brain Res 36: 129–141
Horne MK, Porter R (1980) The discharges during movement of cells in the ventrolateral thalamus of the conscious monkey. J Physiol (Lond) 304: 349–372
Joffroy AJ, Lamarre Y (1974) Single activity in the ventral lateral thalamus of the unanesthetized monkey. Exp Neurol 42: 1–16
Jones EG, Wise SP, Coulter JD (1979) Differential thalamic relationships of sensory-motor and parietal cortical fields in monkeys. J Comp Neurol 183: 833–882
Kalil K (1981) Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey. J Comp Neurol 195: 25–50
Kievit J, Kuypers HGJM (1975) Subcortical afferents to the frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport. Brain Res 85: 261–266
Kievit J, Kuypers HGJM (1977) Organization of the thalamocortical connections to the frontal lobe in the rhesus monkey. Exp Brain Res 29: 299–322
Kim R, Nakano K, Jayaraman A, Carpenter MB (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol 169: 263–290
Kuo J, Carpenter MB (1973) Organization of pallidothalamic projections in the rhesus monkey. J Comp Neurol 151: 201–236
Künzle H (1976) Thalamic projections from the precentral motor cortex in Macaca fascicularis. Brain Res 105: 253–267
Lamarre Y, Joffroy AJ (1971) Spontaneous unit activity in the ventrolateral thalamus of the chronic monkey. Int J Neurol 8: 190–197
Lemon RN, van der Burg J (1979) Short-latency peripheral inputs to thalamic neurones projecting to the motor cortex in the monkey. Exp Brain Res 36: 445–462
Macpherson JM, Rasmusson DD, Murphy JT (1980) Activities of neurons in “motor” thalamus during control of limb movement in the primate. J Neurophysiol 44: 11–28
Massion J (1968) Rôle possible de l'activité rythmique du noyau ventrolateral dans Ia prédétermination centrale du mouvement. J Physiol (Paris) 60: 497–498
Mettler FA (1972) The corticothalamic projection: the structural substrate for the control of the thalamus by the cerebral cortex. In: Frigyesi TL, Rinvik E, Yahr MD (eds) Corticothalamic projections and sensorimotor activities. Raven Press, New York, pp 1–19
Nauta WJH, Mehler WR (1966) Projections of the lentiform nucleus in the monkey. Brain Res 1: 3–42
Olszewski J (1952) The thalamus of Macaca mulatta. An atlas for use with the stereotaxic instrument. Karger, Basel
Percheron G (1977) The thalamic territory of cerebellar afferents and the lateral region of the thalamus of the macaque in stereotaxic ventricular coordinates. J Hirnforsch 18: 375–400
Rispal-Padel L (1979) Functional characteristics of the cerebellothalamo-cortical pathway in the cat. In: Massion J, Sasaki K (eds) Cerebello-cerebellar interactions. Elsevier/North Holland, Amsterdam, pp 67–103
Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4: 539–560
Schmied A, Bénita M, Condé H, Dormont JF (1979) Activity of ventrolateral thalamic neurons in relation to a simple reaction time task in the cat. Exp Brain Res 36: 285–300
Shanta TR, Manocha SL, Bourne GH (1968) A stereotaxic atlas of the java monkey brain. Karger, Basel
Sloper JJ, Powell TPS (1979) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Philos Trans R Soc Lond (Biol) 285: 199–226
Smith AM, Hepp-Reymond M-C, Wyss UR (1975) Relation of activity in precentral cortical neurons to force and rate of force change during isometric contractions of finger muscles. Exp Brain Res 23: 315–332
Smith AM, Massion J, Gahéry Y, Roumieu J (1978) Unitary activity of ventrolateral nucleus during placing movement and associated postural adjustment. Brain Res 149: 329–346
Smith AM, Bourbonnais D (1981) Neuronal activity in cerebellar cortex related to control of prehensile force. J Neurophysiol 45: 286–303
Stanton GB (1980) Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: an anterograde degeneration study. J Comp Neurol 190: 699–731
Strick PL (1976a) Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J Neurophysiol 39: 1020–1031
Strick PL (1976b) Activity of ventrolateral thalamic neurons during arm movement. J Neurophysiol 39: 1032–1044
Tracey DJ, Asanuma C, Jones EG, Porter R (1980) Thalamic relay to motor cortex: afferent pathways from brain stem, cerebellum, and spinal cord in monkeys. J Neurophysiol 44: 532–554
Walker AE (1938) The primate thalamus. University Chicago Press, Chicago IL
Wiesendanger R, Wiesendanger M (1985a) The thalamic connections with medial area 6 (supplementary, motor cortex) in the monkey (Macaca fascicularis). Exp Brain Res 59: 91–104
Wiesendanger R, Wiesendanger M (1985b) Cerebellocortical linkage in the monkey as revealed by transcellular labeling with the lectin wheat germ agglutinin conjugated to the marker horseradish peroxidase. Exp Brain Res 59: 105–117
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Anner-Baratti, R., Allum, J.H.J. & Hepp-Reymond, M.C. Neural correlates of isometric force in the “motor” thalamus. Exp Brain Res 63, 567–580 (1986). https://doi.org/10.1007/BF00237479
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DOI: https://doi.org/10.1007/BF00237479