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Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties

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Summary

Neuroanatomical studies have demonstrated that the two major descending pathways from the superior colliculus arise from regionally segregated, distinct, cells of origin. Stimulation and lesion studies have implicated the crossed descending tecto-reticulo-spinal projection in approach movements towards novel stimuli whereas the ipsilateral pathway appears to be involved in the control of avoidance and escape-like behaviours. The present electrophysiological study attempted to characterise the sensory properties of antidromically identified cells of origin of these pathways in anaesthetised rats. We found that the contralaterally projecting predorsal bundle (PDB) efferents were primarily somatosensory while the ipsilateral cuneiform (CNF) projection was primarily visual. PDB cells, mainly found in the intermediate layers, responded principally to vibrissal stimulation with their overlying visual fields optimally stimulated by small dark moving objects in the lower rostral and lateral field. In contrast, most CNF cells were located rostromedially, with the greatest contribution from visual cells responsive to stimuli in the upper rostral field. A significant proportion of these showed no response to small moving dark discs but fired vigorously to ‘looming’ stimuli. Ethological considerations suggest that these are appropriate stimulus characteristics for a system controlling approach and avoidance behaviour in an animal such as the rat where predators generally appear from above and prey is found on the ground.

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References

  • Albers FJ, Meek J, Nieuwenhuys R (1988) Morphometric parameters of the superior colliculus of albino and pigmented rats. J Comp Neurol 274:357–370

    Article  PubMed  CAS  Google Scholar 

  • Bagshaw EV, Evans MH (1976) Measurement of current spread from microelectrodes when stimulating within the nervous system. Exp Brain Res 25:391–400

    Article  PubMed  CAS  Google Scholar 

  • Bell C, Sierra G, Buendia N, Segundo JP (1964) Sensory properties of neurons in the mesencephalic reticular formation. J Neurophysiol 27:961–987

    PubMed  CAS  Google Scholar 

  • Bickford ME, Hall WC (1989) Collateral projections of predorsal bundle cells of the superior colliculus in the rat. J Comp Neurol 283:86–106

    Article  PubMed  CAS  Google Scholar 

  • Bishop PO, Burke W, Davis R (1962) The identification of single units in central visual pathways. J Physiol 162:409–431

    PubMed  CAS  Google Scholar 

  • Bower TGR, Broughton JM, Moore MK (1970) Infant responses to approaching objects: an indicator of response to distal variables. Percept Psychophys 9:193–196

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Chevalier G, Deniau JM (1984) Spatio-temporal organisation of a branched tecto-spinal/tecto-diencephalic neuronal system. Neuroscience 12:427–439

    Article  PubMed  CAS  Google Scholar 

  • Chevalier G, Vacher S, Deniau JM (1984) Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behaviour. Exp Brain Res 53:320–326

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Coles SK, Iles JF, Nicolopoulos-Stournaras S (1989) The mesencephalic centre controlling locomotion in the rat. Neuroscience 28:149–157

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dean P, Redgrave P, Mitchell IJ (1988b) Organisation of efferent projections from superior colliculus to brainstem in rat: evidence for functional output channels. Progr Brain Res 77:27–36

    Article  Google Scholar 

  • Dean P, Redgrave P, Westby GWM (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137–147

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Dykes R, Lamour Y (1988) Neurons without demonstrable receptive fields outnumber neurons having receptive fields in samples from the somatosensory cortex of anaesthetised or paralysed cats and rats. Brain Res 440:133–143

    Article  PubMed  CAS  Google Scholar 

  • Edelman GM, Finkel LH (1984) Neuronal group selection in the cerebral cortex. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 653–695

    Google Scholar 

  • Ellard CG, Goodale MA (1986) The role of the predorsal bundle in head and body movements elicited by electrical stimulation of the superior colliculus in the Mongolian gerbil. Exp Brain Res 64:421–433

    Article  PubMed  CAS  Google Scholar 

  • Ellard CG, Goodale MA (1988) A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil. Exp Brain Res 71:307–319

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Gioia M, Bianchi R (1987) Ultrastructural study of the nucleus cuneiformis in the cat. J Hirnforsch 28:375–383

    PubMed  CAS  Google Scholar 

  • Harris LR, Blakemore C, Donaghy M (1980) Integration of visual and auditory space in the mammalian superior colliculus. Nature 288:56–59

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Harting JK, Huerta MF, Hashikawa T, Weber JT, van Lieshout, DP (1988) Neuroanatomical studies of the nigrotectal projection in the cat. J Comp Neurol 278:615–631

    Article  PubMed  CAS  Google Scholar 

  • Humphrey NK (1968) Responses to visual stimuli in the superior colliculus of rats and monkeys. Exp Neurol 20:312–340

    Article  PubMed  CAS  Google Scholar 

  • Illing RB, Graybiel AM (1986) Complementary and non-matching affrent compartments in the cat's superior colliculus: innervation of the acetylcholinestaerase-poor domain of the intermediate grey layer. Neuroscience 18:373–394

    Article  PubMed  CAS  Google Scholar 

  • Ingle DJ (1982) Organization of visuomotor behaviours in vertebrates. In: Ingle DJ, MA Goodale, RJW Mansfield (eds).Analysis of visual behaviour. MIT Press, Cambridge MA

    Google Scholar 

  • Ingle DJ (1983) Brain mechanisms of visual localisation in frogs and toads. In: Ewert JP, Capranica RR, Ingle DJ (eds)Advances in vertebrate neurobiology. Plenum, New York, pp 177–226

    Google Scholar 

  • Keay KA, Redgrave P, Dean P (1987) Cardiovascular changes elicited by microinjection of N-methyl-D-aspartate into the superior colliculus of the hooded lister rat. Neurosci Lett Suppl 29:S127

    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

    Article  PubMed  CAS  Google Scholar 

  • Keay KA, Westby GWM, Frankland P (1989) Sensory segregation of the cells of origin of the contralateral descending pathway in rat superior colliculus: an electrophysiological analysis. Neurosci Lett Suppl 36:S70

    Google Scholar 

  • Kemel ML, Desban M, Gauchy C, Glowinski J, Besson MJ (1988) Topographical organisation of efferent projections from the cat substantia nigra pars reticulata. Brain Res 455:307–323

    Article  PubMed  CAS  Google Scholar 

  • Killackey HP, Erzurumlu RS (1981) Trigeminal projections to the superior colliculus of the rat. J Comp Neurol 201:221–242

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • King AJ, Palmer AR (1983) Cells responsive to free-field auditory stimuli in guinea pig superior colliculus: distribution and response properties. J Physiol 342:361–381

    PubMed  CAS  Google Scholar 

  • King AJ, Palmer AR (1985) Integration of visual and auditory information in bimodal neurones in the guinea pig superior colliculus. Exp Brain Res 60:492–500

    Article  PubMed  CAS  Google Scholar 

  • King SM, Redgrave P, Dean P (1989) Defensive reactions to peripheral visual stimuli in humans. Neurosci Lett Suppl 36:S69

    Google Scholar 

  • Lemon R (1984) Methods for neuronal recording in conscious animals. IBRO series: methods in the neurosciences, Vol 4. Wiley, Chichester

    Google Scholar 

  • Lipski J (1981) Antidromic activation of neurones as an analytic tool in the study of the central nervous system. J Neurosci Meth 4:1–32

    Article  CAS  Google Scholar 

  • Marrow LP, Redgrave P (1989) Topographical organisation of the nigrotectal pathway in rat. Neurosci Lett Suppl 36:S10

    Google Scholar 

  • McHaffie JG, Kao CQ, Stein BE (1989) Nociceptive neurons in rat superior colliculus: response properties, topography and functional implications. J Neurophysiol 62:510–525

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1985) Descending efferents from the superior colliculus relay integrated multisensory information. Science 227:657–659

    PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1986) Visual, auditory and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol 56:640–662

    PubMed  CAS  Google Scholar 

  • Mitchell IJ, Redgrave P, Dean P (1988) Plasticity of behavioral response to repeated injection of glutamate in cuneiform area of rat. Brain Res 460:394–397

    Article  PubMed  CAS  Google Scholar 

  • Murray EA, Coulter JD (1982) Organisation of tecto-spinal neurons in the cat and rat superior colliculus. Brain Res 243:201–214

    Article  PubMed  CAS  Google Scholar 

  • Northmore DPM, Levine ES, Schneider GE (1988) Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595–605

    Article  PubMed  CAS  Google Scholar 

  • Palmer AR, King AJ (1982) The representation of auditory space in the mammalian superior colliculus. Nature 299:248–249

    Article  PubMed  CAS  Google Scholar 

  • Papez JW, Freeman GL (1930) Superior colliculi and their fibre connections in the rat. J Comp Neurol 51:409–439

    Article  Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, Sydney

    Google Scholar 

  • Pellegrino LJ, Pellegrino AS, Cushman AJ (1979) A stereotaxic atlas of the rat brain, 2nd edn. Plenum Press, New York

    Google Scholar 

  • Petrovicky P (1876) Projections from the tectum mesencephali to brain stem structures in the rat. Folia Morphol 24:41–48

    Google Scholar 

  • Ranck JB (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Regan D, Beverley KI (1987) Looming detectors in the human visual pathway. Vision Res 18:415–421

    Article  Google Scholar 

  • Rhoades RW, DellaCroce DD (1980) Cells of origin of the tectospinal tract in the golden hamster: an anatomical and electrophysiological investigation. Exp Neurol 67:163–180

    Article  PubMed  CAS  Google Scholar 

  • Rhoades RW, Mooney RD, Klein BG, Jacquin MF, Szczepanik AM, Chiaia NL (1987) The structural and functional characteristics of tectospinal neurons in the golden hamster. J Comp Neurol 255:451–465

    Article  PubMed  CAS  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 250:482–524

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schiff W (1965) Perception of impending collision: a study of visually directed avoidant behaviour. Psychol Monogr Gen Appl 79:1–26

    Google Scholar 

  • Schneider GE (1969) Two visual systems. Science 163:895–902

    PubMed  CAS  Google Scholar 

  • Siminoff R, Schwassmann HO, Kruger L (1966) An electrophysiological study of the visual projection to the superior colliculus of the rat. J Comp Neurol 127:435–444

    Article  PubMed  CAS  Google Scholar 

  • Sparks DL (1986) Translation of sensory signals into commands for the control of saccadic eye-movements: role of the superior colliculus. Ann Rev Neurosci 66:118–171

    CAS  Google Scholar 

  • Sprague JM, Meikle TH (1965) The role of the superior colliculus in visually guided behaviour. Exp Neurol 11:115–146

    Article  PubMed  CAS  Google Scholar 

  • Sprague JM, Berlucchi G, Rizzolatti G (1973) The role of the superior colliculus and pretectum in vision and visually guided behaviour. In: Jung R (ed) Handbook of sensory physiology, Vol VIII/3B. Springer, Berlin

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Waldron HA, Gwyn DG (1969) Descending nerve tracts in the spinal cord of the rat. I. Fibres from the midbrain. J Comp Neurol 137:143–154

    Article  PubMed  CAS  Google Scholar 

  • Westby GWM, Redgrave P, Dean P (1988) Electrophysiological characterisation of collicular output pathways mediating approach and avoidance in the rat. Neurosci Lett Suppl 32:S39

    Google Scholar 

  • Zemlan FP and Behbehani MM (1988) Nucleus cuneiformis and pain modulation: anatomy and behavioural pharmacology. Brain Res 453:89–102

    Article  PubMed  CAS  Google Scholar 

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Author notes

  1. K. A. Keay

    Present address: Brain Behaviour Laboratory, Department of Anatomy, University of Sydney, 2006, New South Wales, Australia

  2. M. Bannister

    Present address: Department of Experimental Psychology, Oxford University, South Parks Rd., OX1 3PT, Oxford, UK

Authors and Affiliations

  1. Department of Psychology, University of Sheffield, S10 2TN, Sheffield, UK

    G. W. M. Westby, K. A. Keay, P. Redgrave, P. Dean & M. Bannister

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  1. G. W. M. Westby
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  2. K. A. Keay
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  3. P. Redgrave
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Westby, G.W.M., Keay, K.A., Redgrave, P. et al. Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties. Exp Brain Res 81, 626–638 (1990). https://doi.org/10.1007/BF02423513

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