Skip to main content
SpringerLink
Log in

Excitotoxic lesions of the superior colliculus preferentially impact multisensory neurons and multisensory integration

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The superior colliculus (SC) plays an important role in integrating visual, auditory and somatosensory information, and in guiding the orientation of the eyes, ears and head. Previously we have shown that cats with unilateral SC lesions showed a preferential loss of multisensory orientation behaviors for stimuli contralateral to the lesion. Surprisingly, this behavioral loss was seen even under circumstances where the SC lesion was far from complete. To assess the physiological changes induced by these lesions, we employed single unit electrophysiological methods to record from individual neurons in both the intact and damaged SC following behavioral testing in two animals. In the damaged SC of these animals, multisensory neurons were preferentially reduced in incidence, comprising less than 25% of the sensory-responsive population (as compared with 49% on the control side). In those multisensory neurons that remained following the lesion, receptive fields were nearly twofold larger, and less than 25% showed normal patterns of multisensory integration, with those that did being found in areas outside of the lesion. These results strongly suggest that the multisensory behavioral deficits seen following SC lesions are the combined result of a loss of multisensory neurons and a loss of multisensory integration in those neurons that remain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Behan M, Kime NM (1996) Intrinsic circuitry in the deep layers of the cat superior colliculus. Vis Neurosci 13:1031–1042

    PubMed  CAS  Google Scholar 

  • Behan M, Appell PP, Graper MJ (1988) Ultrastructural study of large efferent neurons in the superior colliculus of the cat after retrograde labeling with horseradish peroxidase. J Comp Neurol 270:171–184

    Article  PubMed  CAS  Google Scholar 

  • Benson CG, Gross JS, Suneja SK, Potashner SJ (1997) Synaptophysin immunoreactivity in the cochlear nucleus after unilateral cochlear or ossicular removal. Synapse 25:243–257

    Article  PubMed  Google Scholar 

  • Berlucchi G, Sprague JM, Levy J, DiBerardino AC (1972) Pretectum and superior colliculus in visually guided behavior and in flux and form discrimination in the cat. J Comp Physiol Psychol 78:123–172

    Article  PubMed  CAS  Google Scholar 

  • Berson DM, Graybiel AM, Bowen WD, Thompson LA (1991) Evidence for intrinsic expression of enkephalin-like immunoreactivity and opioid binding sites in cat superior colliculus. Neuroscience 43:513–529

    Article  PubMed  CAS  Google Scholar 

  • Bourne JA, Rosa MG (2003) Laminar expression of neurofilament protein in the superior colliculus of the marmoset monkey (Callithrix jacchus). Brain Res 973:142–145

    Article  PubMed  CAS  Google Scholar 

  • Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Annu Rev Neurosci 21:149–86

    Article  PubMed  CAS  Google Scholar 

  • Burnett LR, Stein BE, Chaponis D, Wallace MT (2004) Superior colliculus lesions preferentially disrupt multisensory orientation. Neuroscience 124:535–547

    Article  PubMed  CAS  Google Scholar 

  • Cork RJ, Baber SZ, Mize RR (1998) Calbindin d28-k and parvalbumin-immunoreactive neurons form complementary sublaminae in the rat superior colliculus. J Comp Neurol 394:205–217

    Article  PubMed  CAS  Google Scholar 

  • de Leon M, Covenas R, Narvaez JA, Aguirre JA, Gonzalez-Baron S (1994) Distribution of calbindin D-28k-immunoreactivity in the cat brainstem. Arch Ital Biol 132:229–241

    PubMed  Google Scholar 

  • Eysel UT, Schweigart G (1999) Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. Cereb Cortex 9:101–109

    Article  PubMed  CAS  Google Scholar 

  • Eysel UT, Schweigart G, Mittmann T, Eyding D, Qu Y, Vandesande F, Orban G, Arckens L (1999) Reorganization in the visual cortex after retinal and cortical damage. Restor Neurol Neurosci 15:153–164

    PubMed  CAS  Google Scholar 

  • Freedman EG, Stanford TR, Sparks DL (1996) Combined eye–head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. J Neurophysiol 76:927–952

    PubMed  CAS  Google Scholar 

  • Hanes DP, Wurtz RH (2001) Interaction of the frontal eye field and superior colliculus for saccade generation. J Neurophysiol 85:804–815

    PubMed  CAS  Google Scholar 

  • Harris LR (1980) The superior colliculus and movements of the head and eyes in cats. J Physiol (Lond) 300:367–391

    CAS  Google Scholar 

  • Henkel CK, Fuentes-Santamaria V, Alvarado JC, Brunso-Bechtold JK (2003) Quantitative measurement of afferent layers in the ferret inferior colliculus: DNLL projections to sublayers. Hear Res 177:32–42

    Article  PubMed  Google Scholar 

  • Hikosaka O, Wurtz RH (1983) Effects on eye movements of a GABA agonist and antagonist injected into monkey superior colliculus. Brain Res 272:368–372

    Article  PubMed  CAS  Google Scholar 

  • Huang L, Pallas SL (2001) NMDA antagonists in the superior colliculus prevent developmental plasticity but not visual transmission or map compression. J Neurophysiol 86:1179–1194

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ingham NJ, Thornton SK, McCrossan D, Withington DJ (1998) Neurotransmitter involvement in development and maintenance of the auditory space map in the guinea pig superior colliculus. J Neurophysiol 80:2941–2953

    PubMed  CAS  Google Scholar 

  • Jeon CJ, Hartman MK, Mize RR (1997) Glutamate-like immunoreactivity in the cat superior colliculus and visual cortex: further evidence that glutamate is the neurotransmitter of the corticocollicular pathway. Vis Neurosci 14:27–37

    Article  PubMed  CAS  Google Scholar 

  • Jiang W, Wallace MT, Jiang H, Vaughan JW, Stein BE (2001) Two cortical areas mediate multisensory integration in superior colliculus neurons. J Neurophysiol 85:506–522

    PubMed  CAS  Google Scholar 

  • Jiang W, Jiang H, Stein BE (2002) Two corticotectal areas facilitate multisensory orientation behavior. J Cogn Neurosci 14:1240–1255

    Article  PubMed  Google Scholar 

  • Kadunce DC, Vaughan JW, Wallace MT, Benedek G, Stein BE (1997) Mechanisms of within- and cross-modality suppression in the superior colliculus. J Neurophysiol 78:2834–2847

    PubMed  CAS  Google Scholar 

  • Kadunce DC, Vaughan JW, Wallace MT, Stein BE (2001) The influence of visual and auditory receptive field organization on multisensory integration in the superior colliculus. Exp Brain Res 139:303–310

    Article  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 AJ, Schnupp JW, Carlile S, Smith AL, Thompson ID (1996) The development of topographically-aligned maps of visual and auditory space in the superior colliculus. Prog Brain Res 112:335–350

    PubMed  CAS  Google Scholar 

  • King AJ, Schnupp JW, Thompson ID (1998) Signals from the superficial layers of the superior colliculus enable the development of the auditory space map in the deeper layers. J Neurosci 18:9394–9408

    PubMed  CAS  Google Scholar 

  • Lomber SG, Payne BR, Cornwell P (2001) Role of the superior colliculus in analyses of space: superficial and intermediate layer contributions to visual orienting, auditory orienting, and visuospatial discriminations during unilateral and bilateral deactivations. J Comp Neurol 441:44–57

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • McHaffie JG, Stein BE (1983) A chronic headholder minimizing facial obstructions. Brain Res Bull 10:859–860

    Article  PubMed  CAS  Google Scholar 

  • Meredith MA, Ramoa AS (1998) Intrinsic circuitry of the superior colliculus: pharmacophysiological identification of horizontally oriented inhibitory interneurons. J Neurophysiol 79:1597–1602

    PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1983) Interactions among converging sensory inputs in the superior colliculus. Science 221:389–391

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1986a) Spatial factors determine the activity of multisensory neurons in cat superior colliculus. Brain Res 365:350–354

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1990) The visuotopic component of the multisensory map in the deep laminae of the cat superior colliculus. J Neurosci 10:3727–3742

    PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1996) Spatial determinants of multisensory integration in cat superior colliculus neurons. J Neurophysiol 75:1843–1857

    PubMed  CAS  Google Scholar 

  • Meredith MA, Clemo HR, Stein BE (1991) Somatopic component of the multisensory map in the deep laminae of the cat superior colliculus. J Comp Neurol 312:353–370

    Article  PubMed  CAS  Google Scholar 

  • Middlebrooks JC, Knudsen EI (1984) A neural code for auditory space in the cat’s superior colliculus. J Neurosci 4:2621–2634

    PubMed  CAS  Google Scholar 

  • Mize RR (1992) The organization of GABAergic neurons in the mammalian superior colliculus. Prog Brain Res 90:219–248

    PubMed  CAS  Google Scholar 

  • Mize RR (1996) Neurochemical microcircuitry underlying visual and oculomotor function in the cat superior colliculus. Prog Brain Res 112:35–55

    PubMed  CAS  Google Scholar 

  • Mize RR (1999) Calbindin 28 kD and parvalbumin immunoreactive neurons receive different patterns of synaptic input in the cat superior colliculus. Brain Res 843:25–35

    Article  PubMed  CAS  Google Scholar 

  • Mize RR, Butler GD (2000) The NMDAR1 subunit of the N-methyl-d-aspartate receptor is localized at postsynaptic sites opposite both retinal and cortical terminals in the cat superior colliculus. Vis Neurosci 17:41–53

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Munoz DP, Guitton D (1989) Fixation and orientation control by the tecto-reticulo-spinal system in the cat whose head is unrestrained. Rev Neurol (Paris) 145:567–579

    CAS  Google Scholar 

  • Nadler JV, Cuthbertson GJ (1980) Kainic acid neurotoxicity toward hippocampal formation: dependence on specific excitatory pathways. Brain Res 195:47–56

    Article  PubMed  CAS  Google Scholar 

  • Nitsch R, Bader S, Frotscher M (1992) Reorganization of input synapses of parvalbumin-containing neurons in the rat fascia dentata following entorhinal lesion. Neurosci Lett 135:33–36

    Article  PubMed  CAS  Google Scholar 

  • Okada Y (1992) The distribution and function of gamma-aminobutyric acid (GABA) in the superior colliculus. Prog Brain Res 90:249–262

    PubMed  CAS  Google Scholar 

  • Perrault TJ Jr, Vaughan JW, Stein BE, Wallace MT (2003) Neuron-specific response characteristics predict the magnitude of multisensory integration. J Neurophysiol 90:4022–4026

    Article  PubMed  Google Scholar 

  • Perrault TJ Jr, Vaughan JW, Stein BE, Wallace MT (2005) Superior colliculus neurons use distinct operational modes in the integration of multisensory stimuli. J Neurophysiol 93:2575–2586

    Article  PubMed  Google Scholar 

  • Razak KA, Huang L, Pallas SL (2003) NMDA receptor blockade in the superior colliculus increases receptive field size without altering velocity and size tuning. J Neurophysiol 90:110–119

    Article  PubMed  CAS  Google Scholar 

  • Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415

    Article  PubMed  CAS  Google Scholar 

  • Schiller PH, Stryker M, Cynader M, Berman N (1974) Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. J Neurophysiol 37:181–194

    PubMed  CAS  Google Scholar 

  • Schwarcz R, Hokfelt T, Fuxe K, Jonsson G, Goldstein M, Terenius L (1979) Ibotenic acid-induced neuronal degeneration: a morphological and neurochemical study. Exp Brain Res 37:199–216

    Article  PubMed  CAS  Google Scholar 

  • Sommer MA, Wurtz RH (1998) Frontal eye field neurons orthodromically activated from the superior colliculus. J Neurophysiol 80:3331–3335

    PubMed  CAS  Google Scholar 

  • Sprague JM (1966) Interaction of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science 153:1544–1547

    Article  PubMed  CAS  Google Scholar 

  • Sprague JM (1972) The superior colliculus and pretectum in visual behavior. Invest Ophthalmol 11:473–482

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Stanford TR, Quessy S, Stein BE (2005) Evaluating the operations underlying multisensory integration in the cat superior colliculus. J Neurosci 25:6499–6508

    Article  PubMed  CAS  Google Scholar 

  • Stein BE (1988) Superior colliculus-mediated visual behaviors in cat and the concept of two corticotectal systems. Prog Brain Res 75:37–53

    PubMed  CAS  Google Scholar 

  • Stein BE, Clamann HP (1981) Control of pinna movements and sensorimotor register in cat superior colliculus. Brain Behav Evol 19:180–192

    PubMed  CAS  Google Scholar 

  • Stein BE, Meredith MA (1993) The merging of the senses. MIT Press, Cambridge

    Google Scholar 

  • Stein BE, Goldberg SJ, Clamann HP (1976a) The control of eye movements by the superior colliculus in the alert cat. Brain Res 118:469–474

    Article  PubMed  CAS  Google Scholar 

  • Stein BE, Magalhaes-Castro B, Kruger L (1976b) Relationship between visual and tactile representations in cat superior colliculus. J Neurophysiol 39:401–419

    PubMed  CAS  Google Scholar 

  • Stein BE, Huneycutt WS, Meredith MA (1988) Neurons and behavior: the same rules of multisensory integration apply. Brain Res 448:355–358

    Article  PubMed  CAS  Google Scholar 

  • Stein BE, Meredith MA, Huneycutt WS, McDade L (1989) Behavioral indices of multisensory integration: orientation to visual cues is affected by auditory stimuli. J Cogn Neurosci 1:12–24

    Article  Google Scholar 

  • Tao HW, Poo MM (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45:829–836

    Article  PubMed  CAS  Google Scholar 

  • Wallace MT, Stein BE (1994) Cross-modal synthesis in the midbrain depends on input from cortex. J Neurophysiol 71:429–432

    PubMed  CAS  Google Scholar 

  • Wallace MT, Stein BE (1996) Sensory organization of the superior colliculus in cat and monkey. Prog Brain Res 112:301–311

    Article  PubMed  CAS  Google Scholar 

  • Wallace MT, Stein BE (1997) Development of multisensory neurons and multisensory integration in cat superior colliculus. J Neurosci 17:2429–2444

    PubMed  CAS  Google Scholar 

  • Wallace MT, Stein BE (2000) Onset of cross-modal synthesis in the neonatal superior colliculus is gated by the development of cortical influences. J Neurophysiol 83:3578–3582

    PubMed  CAS  Google Scholar 

  • Wallace MT, Meredith MA, Stein BE (1993) Converging influences from visual, auditory, and somatosensory cortices onto output neurons of the superior colliculus. J Neurophysiol 69:1797–1809

    PubMed  CAS  Google Scholar 

  • Wallace MT, Wilkinson LK, Stein BE (1996) Representation and integration of multiple sensory inputs in primate superior colliculus. J Neurophysiol 76:1246–1266

    PubMed  CAS  Google Scholar 

  • Wallace MT, Meredith MA, Stein BE (1998) Multisensory integration in the superior colliculus of the alert cat. J Neurophysiol 80:1006–1010

    PubMed  CAS  Google Scholar 

  • Wilkinson LK, Meredith MA, Stein BE (1996) The role of anterior ectosylvian cortex in cross-modality orientation and approach behavior. Exp Brain Res 112:1–10

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Nancy London for her editorial assistance. This work was supported by NIH MH63861 and NS36916.

Author information

Author notes

  1. Thomas J. Perrault Jr

    Present address: Department of Neural and Behavioral Sciences, Penn State University College of Medicine, Hershey, PA, 17033, USA

Authors and Affiliations

  1. Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC, 27157, USA

    Luke R. Burnett, Barry E. Stein, Thomas J. Perrault Jr & Mark T. Wallace

  2. Vanderbilt Kennedy Center for Research on Human Development, Department of Hearing and Speech Sciences, Vanderbilt University, 465 21st Avenue South, Nashville, TN, 37232, USA

    Mark T. Wallace

Authors
  1. Luke R. Burnett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barry E. Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas J. Perrault Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark T. Wallace
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark T. Wallace.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burnett, L.R., Stein, B.E., Perrault, T.J. et al. Excitotoxic lesions of the superior colliculus preferentially impact multisensory neurons and multisensory integration. Exp Brain Res 179, 325–338 (2007). https://doi.org/10.1007/s00221-006-0789-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0789-8

Keywords

Search

Navigation