Summary
This study investigated the role of the ventral lateral (VL) nucleus of the thalamus as a lemniscal relay to motor cortex. Intracellular recordings were obtained from thalamic VL relay neurons in cats anesthetized with chloralose, following stimulation of the dorsal column nuclei. VL neurons were identified by their short-latency input from the cerebellar nuclei, their antidromic activation from motor cortex and their anatomical location. A total of 105 neurons was studied. The occurence of temporal facilitation to double volleys was also examined. It was found that 80/105 (75%) neurons responded with excitation and/or inhibition to stimulation of the dorsal column nuclei. The latencies of the postsynaptic responses ranged from 2.0 to 20 ms (median 10.0 ms). The latencies of nearly all responses (79/80) were > 3 ms and nearly all responses (45/47) which were tested for it, displayed temporal facilitation to double shock stimulation, consistent with polysynaptic transmission. Effective stimulation sites were found in the gracile and cuneate nuclei. Recording sites were located throughout VL, including the “border region” with the ventral posterior lateral nucleus (VPL). There was no obvious topographic relationship between location of recording site and latency or polarity (excitation versus inhibition) of the synaptic responses. This is consistent with dorsal column input diffusely distributed over VL. When the recording electrodes penetrated VPL, characteristics of the EPSPs were indicative of monosynaptic transmission (short latency, no temporal facilitation). This clear transition from VL to VPL suggests that it is not necessary to define, on physiological grounds, a separate “border region” between these two nuclei. The data provide evidence that dorsal column information reaches VL neurons polysynaptically, not monosynaptically. This indicates that VL is part of a long-latency, not short-latency path through the dorsal column nuclei to motor cortex.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andersen P, Eccles JC, Schmidt RF, Yokota T (1964) Identification of relay cells and interneurons in the cuneate nucleus. J Neurophysiol 27: 1080–1095
Anderson ME, DeVito JL (1987) An analysis of potentially converging inputs to the rostral ventral thalamic nuclei of the cat. Exp Brain Res 68: 260–276
Appelberg B (1961) Localization of focal potentials evoked in the red nucleus and ventrolateral nucleus of the thalamus by electrical stimulation of the cerebellar nuclei. Acta Physiol Scand 51: 356–370
Asanuma H (1981) Functional role of sensory inputs to the motor cortex. Progr Neurobiol 16: 241–262
Asanuma H, Rosen I (1973) Spread of mono- and polysynaptic connections within cat's motor cortex. Exp Brain Res 16: 507–520
Asanuma H, Larsen K, Zarzecki P (1979) Peripheral input pathways projecting to the motor cortex in the cat. Brain Res 172: 197–208
Asanuma H, Larsen K, Yumiya H (1980) Peripheral input pathways to the monkey motor cortex. Exp Brain Res 38: 349–355
Bagshaw EV, Evans MH (1976) Measurement of current spread from microelectrodes when stimulating within the nervous system. Exp Brain Res 25: 391–400
Berkley KJ (1983) Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brain stem of cats and monkeys. II. Cerebellar projections compared with those of the ascending somatic sensory pathways in lateral diencephalon. J Comp Neurol 220: 229–251
Berkley KJ, Budell RJ, Blomqvist A, Bull M (1986) Output systems of the dorsal column nuclei in the cat. Brain Res Rev 11: 199–225
Berman AL (1968) The brain stem of the cat. The University of Wisconsin Press, Madison Wisconsin
Brinkmann J, Bush BM, Porter R (1978) Deficient influences of peripheral stimuli on precentral neurones in monkeys with dorsal column lesions. J Physiol 276: 27–48
Craig AD, Burton H (1985) The distribution and topographical organization in the thalamus of anterogradely-transported horse radish peroxidase after spinal injections in cat and raccoon. Exp Brain Res 58: 227–254
Dykes RW, Rasmusson DD, Sretavan 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
Dykes RW, Herron P, Lin CS (1986) Ventroposterior thalamic regions projecting to cytoarchitectonic areas 3a and 3b in the cat. J Neurophysiol 56: 1521–1541
Eccles JC (1964) The physiology of synapses. Springer, New York
Gordon G, Seed WA (1961) An investigation of the nucleus gracilis of the cat by antidromic stimulation. J Physiol 155: 589–601
Gordon G, Jukes MGM (1964) Dual organization of the exteroceptive components of the cat's gracile nucleus. J Physiol 173: 263–290
Grant G, Boivie J, Silfvenius H (1973) Course and termination of fibres from the nucleus Z of the medulla oblongata: an experimental light microscopical study in the cat. Brain Res 55: 55–70
Grillner S, Hongo T, Lund S (1970) The vestibulospinal tract. Effects on alphamotoneurones in the lumbosacral spinal cord in the cat. Exp Brain Res 10: 94–120
Hassler R, Muhs-Clement K (1964) Architektonischer Aufbau des somatosensorischen und parietalen Cortex der Katze. J Hirnforsch 6: 679–714
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
Hongo T, Jankowska E (1967) Effects from the sensorimotor cortex on the spinal cord in cats with transsected pyramids. Exp Brain Res 3: 117–134
Jankowska E, Roberts WJ (1972) An electrophysiological demonstration of the axonal projections of single spinal interneurons in the cat. J Physiol 222: 597–622
Jasper HH, Ajmone-Marsan C (1954) A stereotaxic atlas of the cat. National Research Council of Canada, Ottawa
Johansson H, Sylfvenius H (1977) Input from ipsilateral proprio- and exteroceptive hind limb afferents to nucleus Z of the cat medulla oblongata. J Physiol 265: 371–394
Jones EG (1985) The thalamus. Plenum Press, New York London
Kultas-Ilinsky K, Ribak CE, Peterson GM, Oertel WH (1985) A description of the GABAergic neurons and axon terminals in the motor nuclei of the cat thalamus. J Neurosci 5: 1346–1369
Lemon RN, van der Burg J (1979) Short latency peripheral input to thalamic neurones projecting to the motor cortex in the monkey. Exp Brain Res 36: 445–462
Lundberg A, Malmgren K, Schomburg ED (1987) Reflex pathways from group II muscle afferents. 2. Functional characteristics of reflex pathways to alphamotoneurones. Exp Brain Res 65: 282–293
Mackel R, Noda T (1988) Sensory input to cerebellocerebral relay neurons in the cat thalamus. Brain Res 440: 348–351
Mackel R, Noda T (1989) The pretectum as a site for relaying dorsal column input to thalamic VL neurons. Brain Res 476: 135–139
Mackel R, Iriki A, Jorum E, Asanuma H (1991) Neurons in the pretectal area convey spinal input to the motor thalamus of the cat. Exp Brain Res 84: 12–24
Mackel R, Miyashita E (1991) Post-synaptic effects from the dorsal column nuclei in thalamic VL neurons. Soc Neurosci Abstr 247. 3: 622
Mackel R, Iriki A, Brink EE (1992) Spinal input to thalamic VL neurons: evidence for direct spinothalamic efects. J Neurophysiol (in press)
Nakano K, Kohno M, Hasegawa Y, Tokushige A (1985) Cortical and brain stem afferents to the ventral thalamic nuclei of the cat demonstrated by retrograde axonal transport of horseradish peroxidase. J Comp Neurol 231: 102–120
Peterson BW, Filion M, Felpel LP, Abzug C (1975) Responses of medial reticular neurons to stimulation of vestibular nerve. Exp Brain Res 22: 335–350
Perl ER, Whitlock DG, Gentry JR (1962) Cutaneous projection to second order neurons of the dorsal column system. J Neurophysiol 25: 337–358
Rinvik E, Grofova I (1974) Cerebellar projections to the nuclei ventralis lateralis and ventralis anterior thalami. Experimental electron microscopical and light microscopical studies in the cat. Anat Embryol 146: 95–111
Snider RS, Niemer WT (1970) A stereotaxic atlas of the cat brain. The University of Chicago Press, Chicago
Somana R, Walberg F (1980) A re-examination of the cerebellar projections from the gracile, main and external cuneate nuclei in the cat. Brain Res 186: 33–42
Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68: 649–742
Strick PL (1973) Light microscopic analysis of the cortical projection of the thalamic ventrolateral nucleus of the cat. Brain Res 55: 1–24
Sugimoto T, Mizuno N, Itoh K (1981) An autoradiographic study on the terminal distribution of cerebellothalamic fibers in the cat. Brain Res 215: 29–47
Tamai Y, Waters RS, Asanuma H (1984) Caudal cuneate nucleus projection to the direct thalamic relay to motor cortex in cat: an electrophysiological and anatomical study. Brain Res 323: 360–364
Thomas RC, Wilson VJ (1965) Precise localization of Renshaw cells with a new marking technique. Nature 206: 211–213
Uno M, Yoshida M, Hirota I (1970) The mode of cerebello-thalamic relay transmission investigated with intracellular recording from cells of the ventrolateral nucleus of the cat's thalamus. Exp Brain Res 10: 121–139
Waters RS, Tamai Y, Asanuma H (1985) Caudal cuneate nucleus projection to the direct thalamic relay to the motor cortex: an electrophysiological study. Brain Res 360: 361–365
Wiesendanger M, Ruegg DC, Lucier GE (1976) The influence from stretch receptors on cortical cells of area 3a and 4 in monkey. Exp Brain Res Suppl 1: 437–439
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mackel, R., Miyashita, E. Dorsal column input to thalamic VL neurons: an intracellular study in the cat. Exp Brain Res 88, 551–559 (1992). https://doi.org/10.1007/BF00228184
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228184