Abstract
The firing behavior of 47 ventro-posterior thalamus neurons was studied in two alert squirrel monkeys during rotations of whole body, head and trunk. A total of 27 of these neurons (57%) were sensitive to spatial motion of the head irrespective of the mode of motion. These neurons responded similarly when the head moved simultaneously with the trunk, and when the head voluntarily or involuntarily moved on the stationary trunk. These neurons did not respond to rotation of the trunk when the spatial position of the head was fixed. Five neurons (11%) responded only to involuntary movement of the head produced by external force, but were insensitive to voluntary spatial head movement. They also did not respond to spatial motion of the trunk. Totally 15 neurons (32%) were sensitive to spatial motion, which included rotation of the trunk. These neurons responded when the trunk moved alone, and when the trunk moved simultaneously with the head, but were not responsive to spatial movement of the head while the trunk was stationary. We suggest that the vestibulo–thalamo–cortical pathway comprises two distinct functional channels. In one of these channels, cephalokinetic, spatial motion of the head is coded. In the other channel, somatokinetic, motion of the body in space is coded. Each of these channels further consists of two divisions. In the principal division the motion signal is conveyed continuously, irrespective of the behavioral context of motion. In the other auxiliary division the signal only codes movement caused by externally applied force.
This is a preview of subscription content, access via your institution.






References
Akbarian S, Grüsser OJ, Guldin WO (1992) Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus). J Comp Neurol 326:423–441
Anastasopoulos D, Mergner T (1982) Canal-neck interaction in vestibular nuclear neurons of the cat. Exp Brain Res 46:269–280
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 286:237–265
Batschelet E (1981) Circular statistics in biology. Academic Press, London
Becker W, Nasios G, Raab S, Jurgens R (2002) Fusion of vestibular and podokinesthetic information during self-turning towards instructed targets. Exp Brain Res 144:458–474
Bell CC, Grant K (1992) Sensory processing and corollary discharge effects in mormyromast regions of mormyrid electrosensory lobe II. Cell types and corollary discharge plasticity. J Neurophysiol 68:859–875
Beraneck M, Cullen KE (2007) Activity of vestibular nuclei neurons during vestibular and optokinetic stimulation in the alert mouse. J Neurophysiol 98:1549–1565
Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45:852–868
Brandt T, Dieterich M (1994) Vestibular syndromes in the roll plane: topographic diagnosis from brainstem to cortex. Ann Neurol 36:337–347
Bremmer F, Klam F, Duhamel JR, Ben Hamed S, Graf W (2002) Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur J Neurosci 16:1569–1586
Büttner U, Lang W (1979) The vestibulocortical pathway: neurophysiological and anatomical studies in the monkey. Prog Brain Res 50:581–588
Büttner U, Fuchs AF, Markert-Schwab G, Buckmaster P (1991) Fastigial nucleus activity in the alert monkey during slow eye and head movements. J Neurophysiol 65:1360–1371
Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933
Cullen KE, Chen-Huang C, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex II. Eye movement related neurons. J Neurophysiol 70:844–856
Dieterich M, Bartenstein P, Spiegel S, Bense S, Schwaiger M, Brandt T (2005) Thalamic infarctions cause side-specific suppression of vestibular cortex activations. Brain 128:2052–2067
Duensing F, Schaefer KP (1958) Die Aktivität einzelner Neurone im Bereich der Vestibulariskerne bei Horizontalbeschleungungen unter besonderer Berücksichtgung des vestiulären Nystagmus. Arch Psychiatr Nervenkr 198:225–252
Emmers R, Akert K (1963) A stereotaxic atlas of the brain of the squirrel monkey (Saimiri sciureus). The University of Wisconsin press, Madison
Gdowski GT, McCrea RA (1999) Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation. J Neurophysiol 82:436–449
Gdowski GT, McCrea RA (2000) Neck proprioceptive inputs to primate vestibular nucleus neurons. Exp Brain Res 135:511–526
Grüsser OJ, Pause M, Schreiter U (1990) Localization and responses of neurones in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis). J Physiol 430:537–557
Gu Y, Watkins PV, Angelaki DE, DeAngelis GC (2006) Visual and nonvisual contributions to three-dimentional heading selectivity in the medial superior temporal area. J Neurosci 26:73–85
Guldin WO, Grüsser OJ (1998) Is there a vestibular cortex? Trends Neurosci 21:254–259
Guldin WO, Akbarian S, Grüsser OJ (1992) Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus). J Comp Neurol 326:375–401
von Holst E, Mittelstaedt H (1950) Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37:464–476
Jürgens R, Boss T, Becker W (1999) Estimation of self-turning in the dark: comparison between active and passive rotation. Exp Brain Res 128:491–504
Karnath HO, Johannsen L, Broetz D, Kuker W (2005) Posterior thalamic hemorrhage induces “pusher syndrome”. Neurology 64:1014–1019
Kasper J, Schor RH, Wilson VJ (1988) Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stimulation and vestibular-neck interaction. J Neurophysiol 60:1765–1778
Klam F, Graf W (2003) Vestibular response kinematics in posterior parietal cortex neurons of macaque monkeys. Eur J Neurosci 18:995–1010
Lang W, Büttner-Ennever JA, Büttner U (1979) Vestibular projections to the monkey thalamus: an autoradiographic study. Brain Res 177:3–17
Liedgren SR, Milne AC, Schwarz DW, Tomlinson RD (1976) Representation of vestibular afferents in somatosensory thalamic nuclei of the squirrel monkey (Saimiri sciureus). J Neurophysiol 39:601–612
Marchand AR, Manzoni D, Pompeiano O, Stampacchia G (1987) Effects of stimulation of vestibular and neck receptors on Deiters neurons projecting to the lumbosacral cord. Pflugers Archiv Eur J Physiol 409:13–23
Marlinski V, McCrea RA (2005) Firing behavior of ventro-basal thalamic neurons during voluntary and involuntary head movements. Soc Neurosci Abstr 868:6
Marlinski V, McCrea RA (2006) Spatial motion signals coded by vestibulo-thalamic neurons in the alert squirrel monkey. Soc Neurosci Abstr 5048
Marlinski V, McCrea RA (2008) Activity of ventro-posterior thalamus neurons during rotation and translation in the horizontal plane in the alert squirrel monkey. J Neurophysiol 99:2533–2545
Marlinsky VV (1992) Activity of lateral vestibular nucleus neurons during locomotion in the decerebrate guinea pig. Exp Brain Res 90:583–588
Marlinsky VV (1995) The effect of somatosensory stimulation on second-order and efferent vestibular neurons in the decerebrate decerebellate guinea-pig. Neuroscience 69:661–669
Marlinsky VV (1999a) Vestibular and vestibulo-proprioceptive perception of motion in the horizontal plane in blindfolded man—I. Estimations of linear displacement. Neuroscience 90:389–394
Marlinsky VV (1999b) Vestibular and vestibulo-proprioceptive perception of motion in the horizontal plane in blindfolded man—II. Estimations of rotations about the earth-vertical axis. Neuroscience 90:395–401
Marlinsky VV (1999c) Vestibular and vestibulo-proprioceptive perception of motion in the horizontal plane in blindfolded man—III. Route inference. Neuroscience 90:403–411
McCrea RA, Gdowski GT (2003) Firing behaviour of squirrel monkey eye movement-related vestibular nucleus neurons during gaze saccades. J Physiol 546:207–224
McCrea RA, Gdowski GT, Boyle R, Belton T (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82:416–428
Meng H, May PJ, Dickman JD, Angelaki DE (2007) Vestibular signals in primate thalamus: properties and origins. J Neurosci 27:13590–13602
Mergner T, Deecke L, Wagner HJ (1981) Vestibulo-thalamic projection to the anterior suprasylvian cortex of the cat. Exp Brain Res 44:455–458
Mergner T, Siebold C, Schweigart G, Becker W (1991) Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res 85:389–404
Minor LB, Goldberg JM (1991) Vestibular-nerve inputs to the vestibulo-ocular reflex: a functional-ablation study in the squirrel monkey. J Neurosci 11:1636–1648
Mohr C, Roberts PD, Bell CC (2003) The mormyromast region of the mormyrid electrosensory lobe. II. Responses to input from central sources. J Neurophysiol 90:1211–1223
Nagata S (1986) The vestibulothalamic connections in the rat: a morphological analysis using wheat germ agglutinin-horseradish peroxidase. Brain Res 376:57–70
Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142
Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111
Scudder CA, Fuchs AF (1992) Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 68:244–264
Shaikh AG, Ghasia FF, Dickman JD, Angelaki DE (2005) Properties of cerebellar fastigial neurons during translation, rotation, and eye movements. J Neurophysiol 93:853–863
Shiroyama T, Kayahara T, Yasui Y, Nomura J, Nakano K (1999) Projections of the vestibular nuclei to the thalamus in the rat: a Phaseolus vulgaris leucoagglutinin study. J Comp Neurol 407:318–332
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
Stevens ES, Earhart GM (2006) Changes in perception of active but not passive turning following stepping on the rotating treadmill. Exp Brain Res 171:340–346
Waespe W, Henn V (1977) Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 27:523–538
Wilson VJ, Yamagata Y, Yates BJ, Schor RH, Nonaka S (1990) Response of vestibular neurons to head rotations in vertical planes III. Response of vestibulocollic neurons to vestibular and neck stimulation. J Neurophysiol 64:1695–1703
Acknowledgments
Authors are grateful to Michael Graziano and John Jackson for their work in building the experimental setup, and Dr. Timothy Belton for discussion of the material and help in preparation of the manuscript. This research was supported by NIH grant HIDCD DC05056.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marlinski, V., McCrea, R.A. Coding of self-motion signals in ventro-posterior thalamus neurons in the alert squirrel monkey. Exp Brain Res 189, 463–472 (2008). https://doi.org/10.1007/s00221-008-1442-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-008-1442-5
Keywords
- Vestibular
- Thalamus
- Movement
- Neck proprioception
- Self-motion perception