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The projection from superior colliculus to cuneiform area in the rat

II. Defence-like responses to stimulation with glutamate in cuneiform nucleus and surrounding structures

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Summary

To investigate the role of the projection from superior colliculus to the cuneiform nucleus in mediating collicular responses, the cuneiform area (including the cuneiform nucleus and immediately adjacent structures such as caudal central grey) was stimulated in rats with microinjections of glutamate (50 mM, 200 nl, 10 nmole) and the animals' head and body movements observed. The most common responses obtained from sites in the cuneiform area were freezing, darting or fast running, the form or direction of which did not appear to be strongly influenced by the laterality of the injection. These responses were only a subset of those that have been obtained in previous studies from stimulation of the superior colliculus itself: stimulation of the cuneiform area did not give contralaterally directed movements resembling orienting or approach, or ipsilaterally directed movements resembling cringing or shying. It therefore appears that the tectocuneiform projection is likely to be involved only in some of the behaviours appropriate to unexpected stimuli that are mediated by the superior colliculus, namely undirected defensive responses elicited normally by certain kinds of threatening or noxious stimulation. Involvement with such responses would be consistent with an apparent lack of topography in the tectocuneiform projection, and the connections of the cuneiform nucleus with parts of the brain concerned with nociception (see previous paper). It is unclear, however, whether the somatic responses occur in parallel with, or as a result of, autonomic changes that have also been evoked by stimulation of the cuneiform area. One striking feature of stimulating the cuneiform area with glutamate was that at many sites the intensity of the response appeared to increase with successive (one to three) injections. It is possible that this plasticity of response, which can also be obtained from the superior colliculus itself, is related to processes involved in sensitisation or learning of defensive responses.

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References

  • Bandler R (1982) Induction of ‘rage’ following microinjections of glutamate into midbrain but not hypothalamus of cats. Neurosci Lett 30: 183–188

    Google Scholar 

  • Bandler R (1984) Identification of hypothalamic and midbrain periaqueductal grey neurones mediating aggressive and defensive behaviour by intracerebral microinjections of excitatory amino acids. In: Bandler R (ed) Modulation of sensorimotor activity during alterations in behavioral states. Alan R Liss Inc, New York, pp 369–391

    Google Scholar 

  • Bandler R, DePaulis A, Vergnes M (1985) Identification of midbrain neurones mediating defensive behaviour in the rat by microinjections of excitatory amino acids. Behav Brain Res 15: 107–119

    Google Scholar 

  • Bonvallet M, Newman-Taylor A (1967) Neurophysiological evidence for a differential organisation of the mesencephalic reticular formation. Electroenceph Clin Neurophysiol 22: 54–73

    Google Scholar 

  • Brudzynski SM, Houghton PE, Brownlee RD, Mogenson GJ (1986) Involvement of neuronal cell bodies of the mesencephalic locomotor region in the initiation of locomotor activity of freely behaving rats. Brain Res Bull 16: 377–381

    Google Scholar 

  • Chalupa LM (1984) Visual physiology of the mammalian superior colliculus. In: Vanegas H (ed) The comparative neurology of the optic tectum. Plenum Press, New York, pp 775–818

    Google Scholar 

  • Chalupa LM, Rhoades RW (1977) Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus. J Physiol 270: 595–626

    Google Scholar 

  • Chevalier G, Vacher S, Deniau JM, Desban M (1985) Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res 334: 215–226

    Google Scholar 

  • Cools AR, Coolen JMM, Smit JC, Ellenbroek BA (1984) The striato-nigro-collicular pathway and explosive running behaviour: functional interaction between neostriatal dopamine and collicular GABA. Eur J Pharmacol 100: 71–78

    Google Scholar 

  • Cools AR, Ellenbroek BA, van der Heuvel CM (1983) Picrotoxin microinjections into the brain: a model of abrupt withdrawal ‘jumping’ behaviour in rats not exposed to any opiate? Eur J Pharmacol 90: 237–243

    Google Scholar 

  • Coote JH, Hilton SM, Zbrozyna AW (1973) The ponto-medullary area integrating the defence reaction in the cat and its influence on muscle blood flow. J Physiol 229: 257–274

    Google Scholar 

  • Curtis DR, Phillis JW, Watkins JC (1961) Actions of amino acids on the isolated hemisected spinal cord of the toad. Br J Pharmacol 16: 262–283

    Google Scholar 

  • Dean P, Mitchell IJ, Redgrave P (1988a) Contralateral head movements produced by microinjection of glutamate into superior colliculus of rats: evidence for mediation by multiple output pathways. Neuroscience 24: 491–500

    Google Scholar 

  • Dean P, Mitchell IJ, Redgrave P (1988b) Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats. Neuroscience 24: 501–510

    Google Scholar 

  • Dean P, Redgrave P (1984a) The superior colliculus and visual neglect in rat and hamster. I. Behavioural evidence. Brain Res Rev 8: 129–141

    Google Scholar 

  • Dean P, Redgrave P (1984b) The superior colliculus and visual neglect in rat and hamster. III. Functional implications. Brain Res Rev 8: 155–163

    Google Scholar 

  • Dean P, Redgrave P, Mitchell IJ (1988c) Organisation of efferent projections from superior colliculus to brainstem in rat: evidence for functional output channels. In: Hicks TP, Benedek G (eds) Vision within extrageniculo-striate systems. Progress in brain research, Vol 75. Elsevier, Amsterdam (in press)

    CAS  Google Scholar 

  • Dean P, Redgrave P, Sahibzada N, Tsuji K (1986) Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19: 367–380

    Google Scholar 

  • Depoortere R, Bagri A, Di Scala G, Sandner G (1987) Involvement of the mesencephalic locomotor region in negative reinforcement. Neuroscience 22: Suppl S656

    Google Scholar 

  • Dräger UC, Hubel DH (1975) Responses to visual stimulation and relationship between visual, auditory and somatosensory projections to mouse superior colliculus. J Neurophysiol 38: 690–713

    Google Scholar 

  • Finlay BL, Schneps SE, Wilson KG, Schneider GE (1978) Topography of visual and somatosensory projections to the superior colliculus of the golden hamster. Brain Res 142: 223–235

    Google Scholar 

  • Garcia-Rill E (1986) The basal ganglia and the locomotor regions. Brain Res Rev 11: 47–63

    Google Scholar 

  • Goodchild AK, Dampney RAL, Bandler R (1982) A method for evoking physiological responses by stimulation of cell bodies, but not axons of passage, within localised regions of the central nervous system. J Neurosci Meth 6: 351–363

    Google Scholar 

  • Harting JK, Huerta MF (1984) The mammalian superior colliculus: studies of its morphology and connections. In: Vanegas H (ed) The comparative neurology of the optic tectum. Plenum Press, New York, pp 687–773

    Google Scholar 

  • Henkel CK, Edwards SB (1978) The superior colliculus control of pinna movements in the cat: possible anatomical connections. J Comp Neurol 182: 763–776

    Google Scholar 

  • Hilton SM (1982) The defence-arousal system and its relevance for circulatory and respiratory control. J Exp Biol 100: 159–174

    Google Scholar 

  • Imperato A, Di Chiara G (1981) Behavioural effects of GABA-agonists and antagonists infused in the mesencephalic reticular formation-deep layers of superior colliculus. Brain Res 224: 185–194

    Google Scholar 

  • Kaczmarek LK, Adey WR (1974) Some chemical and electrophysiological effects of glutamate in cerebral cortex. J Neurobiol 5: 231–241

    Google Scholar 

  • Keay KA, Redgrave P, Dean P (1987) Cardiovascular changes elicited by microinjection of N-methyl-D-aspartate (NMDA) into the superior colliculus of the hooded Lister rat. Neurosci Lett Suppl 26: S238

    Google Scholar 

  • Keay KA, Redgrave P, Dean P (1988) Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus. Brain Res Bull 20: 13–26

    Google Scholar 

  • Kilpatrick IC, Collingridge GL, Starr MS (1982) Evidence for the participation of γ-aminobutyiate containing neurons in striatal and nigral derived circling in the rat. Neuroscience 7: 207–222

    Google Scholar 

  • Larson MA, McHaffie JG, Stein BE (1987) Response properties of nociceptive and low-threshold mechanoreceptive neurons in the hamster superior colliculus. J Neurosci 7: 547–564

    Google Scholar 

  • May PJ, Vidal P-P, Baker R (1985) Electrophysiology of the paralemniscal-facial pathway. Soc Neurosci Abstr 11: 82

    Google Scholar 

  • McBean GJ, Roberts PJ (1985) Neurotoxicity of L-glutamate and DL-threo-3-hydroxyaspartate in the rat striatum. J Neurochem 44: 247–254

    Google Scholar 

  • McHaffie JG, Stein BE (1982) Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247: 243–253

    Google Scholar 

  • McMahon SB, Wall PD (1985) Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat. Brain Res 333: 19–26

    Google Scholar 

  • Mel'nikova ZL (1975) Locomotion of rats induced by stimulation of the mesencephalon. Bull Moscow Univ (Biol) 30: 45–51 (in Russian)

    Google Scholar 

  • Mushiake S, Shosaku A, Kayama Y (1984) Inhibition of thalamic ventrobasal complex neurons by glutamate infusion into the thalamic reticular nucleus in rats. J Neurosci Res 12: 93–100

    Google Scholar 

  • Parker SM, Sinnamon HM (1983) Forward locomotion elicited by electrical stimulation in the diencephalon and mesencephalon of the awake rat. Physiol Behav 31: 581–587

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, Sydney

    Google Scholar 

  • Pope SG, Dean P (1979) Hyperactivity, aphagia and motor disturbance following lesions of superior colliculus and underlying tegmentum in rats. Behav Neural Biol 27: 433–453

    Google Scholar 

  • Puil E (1981) S-glutamate: its interactions with spinal neurons. Brain Res Rev 3: 229–322

    Google Scholar 

  • Redgrave P, Dean P (1985) Tonic desynchronization of cortical electroencephalogram by electrical and chemical stimulation of superior colliculus and surrounding structures in urethane-anaesthetised rats. Neuroscience 16: 659–671

    Google Scholar 

  • Redgrave P, Dean P, Mitchell IJ, Odekunle A, Clark A (1988) The projection from superior colliculus to cuneiform area in the rat. I. Anatomical studies. Exp Brain Res 72: 611–625

    Google Scholar 

  • Redgrave P, Dean P, Souki W, Lewis G (1981) Gnawing and changes in reactivity produced by microinjections of picrotoxin into the superior colliculus of rats. Psychopharmacology 75: 198–203

    Google Scholar 

  • Redgrave P, Mitchell IJ, Dean P (1987a) Descending projections from the superior colliculus in rat: a study using orthograde transport of wheatgerm-agglutinin conjugated horseradish peroxidase. Exp Brain Res 68: 147–167

    Google Scholar 

  • Redgrave P, Mitchell IJ, Dean P (1987b) Further evidence for segregated output channels from superior colliculus in rat: ipsilateral tecto-pontine and tecto-cuneiform projections have different cells of origin. Brain Res 413: 170–174

    Google Scholar 

  • Redgrave P, Odekunle A, Dean P (1986) Tectal cells of origin of predorsal bundle cells in rat: location and segregation from ipsilateral descending pathway. Exp Brain Res 63: 279–293

    Google Scholar 

  • Rhoades RW (1981) Organization of somatosensory input to the deep collicular laminae in hamster. Behav Brain Res 3: 201–222

    Google Scholar 

  • Rhoades RW, Mooney RD, Jacquin MF (1983) Complex somatosensory receptive fields of cells in the deep laminae of the hamster's superior colliculus. J Neurosci 3: 1342–1354

    Google Scholar 

  • Ross CA, Ruggiero DA, Park DH, Joh TH, Sved AF, Fernandez-Pardel J, Saavedra JM, Reis DJ (1982) Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J Neurosci 4: 474–494

    Google Scholar 

  • Ross GS, Sinnamon HM (1984) Forelimb and hindlimb stepping by the anesthetized rat elicited by electrical stimulation of the pons and medulla. Physiol Behav 33: 201–208

    Google Scholar 

  • Ruth RE, Rosenfeld JP (1977) Tonic reticular activating system: relationship to aversive brain stimulation effects. Exp Neurol 57: 41–56

    Google Scholar 

  • Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259: 482–524

    Google Scholar 

  • Sahibzada N, Dean P, Redgrave P (1986) Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci 6: 723–733

    Google Scholar 

  • Schiller PH (1985) The superior colliculus and visual function. In: Darien-Smith I (ed) Handbook of physiology — the nervous system, Vol 3. American Physiological Society, Bethesda, pp 457–505

    Google Scholar 

  • Simson EL, Gold RM, Standish LJ, Pallett PL (1977) Axonsparing lesion technique: the use of monosodium-L-glutamate and other amino acids. Science 198: 515–517

    Google Scholar 

  • Sinnamon HM (1984) Forelimb and hindlimb stepping by the anesthetized rat elicited by electrical stimulation of the diencephalon and mesencephalon. Physiol Behav 33: 191–199

    Google Scholar 

  • Stein BE (1981) Organization of the rodent superior colliculus; some comparisons with other mammals. Behav Brain Res 3: 175–188

    Google Scholar 

  • Stein BE, Dixon JP (1979) Properties of superior colliculus neurons in the golden hamster. J Comp Neurol 183: 269–284

    Google Scholar 

  • Tiao Y-C, Blakemore C (1976) Functional organization of the superior colliculus of the golden hamster. J Comp Neurol 168: 483–503

    Google Scholar 

  • Waldbillig RJ (1975) Attack, eating, drinking, and gnawing elicited by electrical stimulation of rat mesencephalon and pons. J Comp Physiol Psychol 89: 200–212

    Google Scholar 

  • Watkins JC (1978) Excitatory amino acids. In McGeer EG, Olney JW, McGeer PL (eds) Kainic acid as a tool in neurobiology. Raven Press, New York, pp 37–69

    Google Scholar 

  • Weldon DA, Calabrese LC, Nicklaus KJ (1983) Rotational behaviour following cholinergic stimulation of the superior colliculus in rats. Pharmacol Biochem Behav 19: 813–820

    Google Scholar 

  • Willette RN, Barcas PP, Krieger AJ, Sapru HN (1983) Vasopressor and depressor areas in the rat medulla. Neuropharmacology 22: 1071–1079

    Google Scholar 

  • Wurtz RH, Albano JE (1980) Visual-motor function of the primate superior colliculus. Ann Rev Neurosci 3: 189–226

    Google Scholar 

  • Yardley CP, Hilton SM (1986) The hypothalamic and brainstem areas from which the cardiovascular and behavioural components of the defence reaction are elicited in the rat. J Auton Nerv Syst 15: 227–244

    Google Scholar 

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  1. I. J. Mitchell

    Present address: Department of Cell and Structural Biology, Stopford Building, Oxford Road, M13 9PT, Manchester, UK

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  1. Department of Psychology, University of Sheffield, S102TN, Sheffield, UK

    I. J. Mitchell, P. Dean & P. Redgrave

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Mitchell, I.J., Dean, P. & Redgrave, P. The projection from superior colliculus to cuneiform area in the rat. Exp Brain Res 72, 626–639 (1988). https://doi.org/10.1007/BF00250607

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