Summary
The intralaminar thalamus of anesthetized rats was explored for neurons activated by stimulation of the superior colliculus and responsive to sensory inputs. Neurons activated by stimulation of the intermediate and deep collicular layers were distributed throughout the intralaminar thalamus. Approximately one half of them responded to tectal as well as sensory inputs. The majority were nociceptive or had a more complex response pattern including responses to auditory stimulation. A smaller population of low threshold units had contralateral orofacial receptive fields and responded to light taps; these units were preferentially localized anteriorly in the central lateral and paracentral nuclei. Neurons responsive to tectal and sensory stimulation were randomly intermingled with other neurons which had no detectable sensory input. The results indicate that ascending projection neurons of the intermediate and deep layers of the superior colliculus provide an input to functionally diverse subpopulations of intralaminar thalamic neurons. In view of its projections to motor cortex and basal ganglia, the intralaminar thalamus appears directly implicated in basal ganglia and superior colliculus related mechanisms of attention, arousal and postural orienting.
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References
Abrahams VC, Clinton RJ, Downey D (1988) Somatosensory projections to the superior colliculus of the anaesthetized cat. J Physiol 396: 563–580
Ahlenius S, Andén NE, Grabowska-Andén M (1982) Apomorphine-induced ipsilateral turning in rats with unilateral lesions of the parafascicular nucleus. Exp Brain Res 47: 270–276
Albano JE, Wurtz RH (1982) Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior-medial thalamus. J Neurophysiol 48: 318–337
Albe-Fessard D, Besson JM (1973) Convergent thalamic and cortical projections — The non-specific system. In: Iggo A (eds) Handbook of sensory physiology. Springer, Berlin, pp 489–560
Albe-Fessard D, Kruger L (1962) Duality of unit discharges from cat centrum medianum in response to natural and electrical stimulation. J Neurophysiol 25: 3–20
Albe-Fessard D, Berkeley KJ, Kruger L, Ralston HJ III, Willis WD Jr (1985) Diencephalic mechanisms of pain sensation. Brain Res Rev 9: 217–296
Aldes LD (1988) Thalamic connectivity of rat somatic motor cortex. Brain Res Bull 20: 333–348
Auroy P, Irthum B, Woda A (1991) Oral nociceptive activity in the rat superior colliculus. Brain Res 549: 275–284
Barth TM, Jones TA, Schallert T (1990) Functional subdivisions of the rat somatic sensorimotor cortex. Behav Brain Res 39: 73–95
Bentivoglio M, Macchi G, Albanese A (1981) The cortical projections of the thalamic intralaminar nuclei, as studied in cat and rat with the multiple fluorescent retrograde tracing technique. Neurosci Lett 26: 5–10
Bentivoglio M, Molinari M, Minchiacchi D, Macchi G (1983) Organization of the cortical projections of the posterior complex and intralaminar nuclei of the thalamus as studied by means of retrograde tracers. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory integration in the thalamus. Elsevier, Amsterdam, pp 337–364
Berendse HW, Groenewegen HJ (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299: 187–228
Bickford ME, Hall WC (1989) Collateral projections of predorsal bundle cells of the superior colliculus in the rat. J Comp Neurol 283: 86–106
Bruce LL, McHaffie JG, Stein BE (1987) The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labeling study with fluorescent dyes. J Comp Neurol 262: 315–330
Burton H, Craig ADJ (1983) Spinothalamic projections in cat, racoon and monkey: a study based on anterograde transport of horseradish peroxidase. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory integration in the thalamus. Elsevier, Amsterdam, pp 17–42
Carli M, Jones GH, Robbins TW (1989) Effects of unilateral dorsal and ventral striatal dopamine depletion on visual neglect in the rat: a neural and behavioural analysis. Neuroscience 29: 309–327
Chevalier G, Deniau JM (1984) Spatio-temporal organization of a branched tecto-spinal/tecto-diencephalic neuronal system. Neuroscience 12: 427–439
Chevalier G, Vacher S, Deniau JM, Albe-Fessard D (1984) Tonic nigral control of tecto spinal/tecto diencephalic branched neurons: a possible implication of basal ganglia in orienting behavior. In: McKenzie JS, Kemm RE, Wilcock LN (eds) The basal ganglia. Plenum Press, New York, pp 247–259
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
Cicirata F, Angaut P, Cioni M, Serapide MF, Papale A (1986) Functional organization of thalamic projections to the motor cortex: an antomical and electrophysiological study in the rat. Neuroscience 19: 81–99
Condé F, Audinat E, Maire-Lepoivre E, Crépel F (1990) Afferent connections of the medial frontal cortex of the rat: a study using retrograde transport of fluorescent dyes. I. Thalamic afferents. Brain Res Bull 24: 341–354
Cowey A, Bozek T (1974) Contralateral “neglect” after unilateral dorsomedial prefrontal lesions in rats. Brain Res 72: 53–63
Dean P, Redgrave P, Westby GWM (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12: 137–147
Dong WK, Ryu H, Wagman IH (1978) Nociceptive responses of neurons in medial thalamus and their relationship to spinothalamic pathways. J Neurophysiol 41: 1592–1613
Donoghue JP, Wise SP (1982) The motor cortex of the rat: Cytoarchitecture and microstrimulation mapping. J Comp Neurol 212: 76–88
Dostrovsky JO, Guilbaud G (1990) Nociceptive responses in medial thalamus of the normal and arthritic rat. Pain 40: 93–104
Drager UC, Hubel D (1975) Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. J Neurophysiol 38: 690–713
Dubé L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267: 455–471
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
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: 224–235
Gioanni Y, Lamarche M (1985) A reappraisal of rat motor cortex organization by intracortical microstimulation. Brain Res 344: 49–61
Glenn LL, Steriade M (1982) Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states. J Neurosci 2: 1387–1404
Graham J, Berman N (1981) Origins of the pretectal and tectal projections to the central lateral nucleus in the cat. Neurosci Lett 26: 209–214
Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tectobulbo-spinal tract. Exp Brain Res 46: 243–256
Groenewegen HJ (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24: 379–431
Grunwerg BS, Krauthamer GM (1990) Vibrissa-responsive neurons of the superior colliculus that project to the intralaminar thalamus of the rat. Neurosci Lett 111: 23–27
Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66: 23–38
Heilman KM, Watson RT (1977) The neglect syndrome: A unilateral defect of the orienting response. In: Harnad S, Doty RW, Goldstein L, Jaynes J, Krauthamer G (eds) Lateralization in the nervous system. Academic Press, New York, pp 285–302
Herkenham M (1980) Laminar organization of thalamic projections to the rat neocortex. Science 207: 532–535
Herkenham M (1986) New perspectives on the organization and evolution of nonspecific thalamocortical projections. In: Jones EG, Peters A (eds) Cerebral cortex. Plenum, New York, pp 403–445
Holstege G, Collewijn H (1982) The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. J Comp Neurol 209: 139–175
Huerta MF, Harting JK (1984) The mammalian superior colliculus: studies of its morphology and connections. In: Venegas H (eds) Comparative neurology of the optic tectum. Plenum, New York, pp 687–773
Huerta MF, Frankfurter A, Harting JK (1983) Studies of the principal sensory and spinal trigeminal nuclei of the rat: projections to the superior colliculus, inferior olive, and cerebellum. J Comp Neurol 220: 147–167
Hunsperger RW, Roman D (1976) The integrative role of the intralaminar system of the thalamus in visual orienting and perception in cat. Exp Brain Res 25: 231–246
Jones EG (1985) The thalamus. Plenum, New York
Kao CQ, McHaffie JG, Meredith MA, Clemo HR, Stein BE (1990) Comparative magnification of the vibrissa representation in the superior colliculus of rodents and cats. Soc Neurosci Abstr 16: 223
Kaufman EFS, Rosenquist AC (1985a) Afferent connections of the thalamic intralaminar nuclei in the cat. Brain Res 335: 281–296
Kaufman EFS, Rosenquist AC (1985b) Efferent projections of the thalamic intralaminar nuclei in the cat. Brain Res 335: 257–279
Kirvel RD (1975) Sensorimotor responsiveness in rats with unilateral superior collicular and amygdaloid lesions. J Comp Physiol Psychol 89: 882–891
Kolb B (1984) Functions of the frontal cortrex of the rat: a comparative review. Brain Res Rev 8: 65–98
Krauthamer GM (1979) Sensory functions of the neostriatum. In: Divac I, Oberg GE (eds) The neostriatum. Pergamon Press, Oxford, pp 263–289
Krauthamer GM, Yamasaki DS, Rhoades RW (1987) Does the neostriatum self-regulate its sensory input? The role of the superior colliculus. In: Schneider JS, Lidsky TI (eds) Basal ganglia and behavior: sensory aspects of motor functioning. Hans Huber, Toronto, pp 17–26
Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171: 157–192
Larson MA, McHaffie JG, Stein BA (1987) Response properties of nociceptive and low-threshold mechanoreceptive neurons in the hamster superior colliculus. Neuroscience 7: 547–564
Leichnetz GR, Gonzalo-Ruiz A (1987) Collateralization of frontal eye field (medial precentral/anterior cingulate) neurons projecting to the paraoculomotor region, superior colliculus, and medial pontine reticular formation in the rat: a fluorescent double-labeling study. Exp Brain Res 68: 355–364
Lim RKS, Krauthamer G, Guzman F, Fulp RR (1969) Central nervous system activity associated with the pain evoked by bradykinin and its alteration by morphine and aspirin. Proc Nat Acad Sci 63: 705–712
Ljungberg T, Ungerstedt U (1976) Sensory inattention produced by 6-hydroxydopamine degeneration of ascending dopamine neurons in the brain. Exp Neurol 53: 585–600
May PJ, Hall WC (1986) The sources of the nigrotectal pathway. Neuroscience 19: 159–180
McGuiness CM, Krauthamer GM (1980) The afferent projections to the centrum medianum of the cat as demonstrated by retro grade transport of horseradish peroxidase. Brain Res 184: 255–269
McHaffie JG, Stein BA (1982) Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247: 243–253
McHaffie JG, Kao C-Q, Stein BE (1989) Nociceptive neurons in rat superior colliculus: response properties, topography, and functional implications. J Neurophysiol 62: 510–525
Miguel-Hidalgo J-J, Senba E, Matsutani S, Takatsuji K, Fukui H, Tohyama M (1989) Laminar and segregated distribution of immunoreactivities for some neuropeptides and adenosine deaminase in the superior colliculus of the rat. J Comp Neurol 280: 410–423
Moschovakis AK, Karabelas AB (1985) Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat. J Comp Neurol 239: 276–308
Orem J, Schlag-Rey M, Schlag J (1973) Unilateral visual neglect and thalamic intralaminar lesions in the cat. Exp Neurol 40: 784–797
Passingham RE, Myers C, Rawlins N, Lightfoot V, Fearn S (1988) Premotor cortex in the rat. Behav Neurosci 102: 101–109
Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates, 1 edn. Academic Press, Sidney
Peschanski M (1984) Trigeminal afferents to the diencephalon in the rat. Neuroscience 12: 465–487
Peschanski M, Besson JM (1984) A spino-reticulo-thalamic pathway in the rat: an anatomical study with reference to pain transmission. Neuroscience 12: 165–178
Peschanski M, Guilbaud G, Gautron M (1981) Posterior intralaminar region in rat: neuronal responses to noxious and non-noxious cutaneous stimuli. Exp Neurol 72: 226–238
Porter LL, White EL (1983) Afferent and efferent pathways of the vibrissal region of primary motor cortex in the mouse. J Comp Neurol 214: 279–289
Posner MI, Presti DE (1987) Selective attention and cognitive control. Trends Neurosci 10: 13–17
Prieto-Gomez B, Dafny N, Reyes-Vazquez C (1989) Dorsal raphe stimulation, 5-HT and morphine microiontophoresis effects on noxious and nonnoxious identified neurons in the medial thalamus of the rat. Brain Res Bull 22: 937–943
Qiao J-T, Skolnick M, Dafny N (1988) Dorsal raphe and external electrical stimulation modulate noxious input to single neurons in nucleus parafascicularis thalami. Brain Res Bull 21: 671–675
Redgrave P, Odekunle A, Dean P (1986) Tectal cells of origin of predorsal bundle in rat: location and segregation from ipsilateral descending pathway. Exp Brain Res 63: 279–293
Reep RL, Corwin JV, Hashimoto A, Watson RT (1984) Afferent connections of medial precentral cortex in the rat. Neurosci Lett 44: 247–252
Reyes-Vazquez C, Prieto-Gomez B, Dafny N (1989) Noxious and non-noxious responses in the medial thalamus of the rat. Neurol Res 11: 177–180
Rhoades RW, Kuo DC, Polcer JD, Fish SE, Voneida TJ (1982) Indirect visual cortical input to the deep layers of the hamster's superior colliculus via the basal ganglia. J Comp Neurol 208: 239–254
Rhoades RW, Mooney RD, Jacquin MF (1983) Complex somatosensory receptive fields of cells in the deep laminae of the hamster's superior colliculus. Neuroscience 3: 1342–1354
Rhoades RW, Mooney RD, Klein BG, Jacquin MF, Szczepanik M, Chiaia NL (1987) The structural and functional characteristics of tectospinal neurons in the golden hamster. J Comp Neurol 255: 451–465
Rhoades RW, Fish SE, Chiaia L, Bennett-Clarke C, Mooney RD (1989) Organization of the projections from the trigeminal brainstem complex to the superior colliculus in the rat and hamster: anterograde tracing with Phaseolus vulgaris leucoagglutinin and intra-axonal injection. J Comp Neurol 289: 641–656
Royce GJ, Mourey RJ (1985) Efferent connections of the centromedian and parafascicular thalamic nuclei: An autoradiographic investigation in the cat. J Comp Neurol 235: 277–300
Sanderson KJ, Welker W, Shambes GM (1984) Reevaluation of motor cortex and of sensorimotor overlap in cerebral cortex of albino rats. Brain Res 292: 251–260
Schlag J, Schlag-Rey M (1984) Visuomotor functions of central thalamus in monkey. II. Unit activity related to visual events, targeting, and fixation. J Neurophysiol 51: 1175–1195
Schlag-Rey M, Schlag J (1977) Visual and presaccadic neuronal activity in thalamic internal medullary lamina of cat: a study of targeting. J Neurophysiol 40: 156–173
Sesack S, Deutsch AY, Roth RH, Bunney BS (1989) Topographical organization of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290: 213–242
Smith Y, Seguela P, Parent A (1987) Distribution of GABAimmunoreactive neurons in the thalamus of the squirrel monkey (Saimiri sciureus). Neuroscience 22: 579–591
Sparks DL (1988) Neural cartography: sensory and motor maps in the superior colliculus. Brain Behav Evol 31: 49–56
Sprague JM, Meikle TH Jr (1965) The role of the superior colliculus in visually guided behavior. Exp Neurol 11: 114–146
Stein BE, Dixon JP (1978) Superior colliculus cells respond to noxious stimuli. Brain Res 158: 65–73
Takada M, Itoh K, Yasui Y, Sugimoto T, Mizuno N (1985) Topographical projections from the posterior thalamic regions to the striatum in the cat, with reference to possible tecto-thalamostriatal connections. Exp Brain Res 60: 385–396
Tehovnik EJ, Spence SJ, Saint-Cyr JA (1989) Efferent projections of the anteromedial cortex of the rat as described by Phaseolus vulgaris leucoagglutinin immunohistochemistry. Behav Brain Res 35: 153–162
Tömböl T, Bentivoglio M, Macchi G (1990) Neuronal cell types in the thalamic intralaminar central lateral nucleus of the cat. Exp Brain Res 81: 491–499
Tokuno H, Nakamura Y (1987) Organization of the nigrotectospinal pathway in the cat: a light and electron microscopic study. Brain Res 436: 76–84
Ullán J (1985) Cortical topography of thalamic intralaminar nuclei. Brain Res 328: 333–340
Van der Kooy D (1979) The organization of the thalamic, nigral and raphe cells projecting to the medial vs lateral caudateputamen in rat: a fluorescent double labeling study. Brain Res 169: 381–387
Vargo JM, Corwin JV, King V, Reep RL (1988) Hemispheric asymmetry in neglect produced by unilateral lesions of dorsomedial prefrontal cortex in rats. Exp Neurol 102: 199–209
Veening JG, Cornelissen FM, Lieven PAJM (1980) The topical organization of the afferents to the caudatoputamen of the rat: a horseradish peroxidase study. Neuroscience 5: 1253–1268
Westby GWM, Keay KA, Redgrave P, Dean P, Bannister M (1990) Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties. Exp Brain Res 81: 626–638
Williams MN, Faull RL (1988) The nigrotectal projection and tectospinal neurons in the rat: a light and electron microscopic study demonstrating a monosynaptic nigral input to identified tectospinal neurons. Neuroscience 25: 533–562
Wurtz RH, Goldberg ME (1971) Superior colliculus cell responses related to eye movements in awake monkeys. Science 171: 82–84
Yamasaki DSG, Krauthamer GM (1990) Somatosensory neurons projecting from the superior colliculus to the intralaminar thalamus in the rat. Brain Res 523: 188–194
Yamasaki DSG, Krauthamer GM, Rhoades RW (1986) Superior collicular projection to intralaminar thalamus in rat. Brain Res 378: 223–233
Yen C-T, Fu T-C, Chen R-C (1989) Distribution of thalamic nociceptive neurons activated from the tail of the rat. Brain Res 498: 118–122
Zainos A, Deanda R, Chavez L, Garcia-Munoz L (1984) Turning behavior, barrel rolling, and sensory neglect induced by picrotoxin in the thalamus. Exp Neurol 83: 534–547
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Grunwerg, B.S., Krauthamer, G.M. Sensory responses of intralaminar thalamic neurons activated by the superior colliculus. Exp Brain Res 88, 541–550 (1992). https://doi.org/10.1007/BF00228183
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DOI: https://doi.org/10.1007/BF00228183