Importance of NMDA receptors for multimodal integration in the deep layers of the cat superior colliculus

J Neurophysiol. 1996 Feb;75(2):920-30. doi: 10.1152/jn.1996.75.2.920.

Abstract

1. Many sensory events contain multimodal information, yet most sensory nuclei are devoted to the analysis of single-modality information. In the deep superior colliculus (DSC), visual, auditory, and somatosensory information converges on individual multimodal neurons. The responses of multimodal neurons are determined by the temporal and spatial correspondence properties of the converging inputs such that stimuli arising from the same event elicit a facilitated multimodal response. 2. N-methyl-D-aspartate (NMDA) receptors may underlie the detection of spatial and temporal coincidence and could be involved in the generation of multimodal facilitatory responses because of the nonlinear properties of NMDA-receptor-mediated events. To assess the role of NMDA receptors in multimodal integration, we made extracellular recordings from single multisensory neurons in the DSC of the cat. 3. The responses to visual, auditory, and somatosensory stimuli alone and to multimodal combinations of stimuli were challenged with iontophoretically applied D-2-amino-5-phosphonovalerate (AP5), an NMDA receptor antagonist. All responses to visual stimuli presented alone (n = 9) were greatly reduced. Somatosensory responses (n = 25) were usually decreased. In contrast, the responses to auditory stimulation were decreased (n = 9), unaffected (n = 3), or enhanced (n = 5). 4. Responses to multimodal stimulus presentations were consistently reduced during iontophoretic application of AP5, irrespective of the modalities that made up the stimulus. The reductions of multimodal responses were significantly greater than the sum of the reductions of responses to single-modality stimuli. 5. The data suggest that for unimodal stimuli, the importance of NMDA receptors in synaptic transmission of sensory responses in DSC may be dependent on the stimulus modality. Furthermore, NMDA receptors are of major importance in the integration of input from different modalities for the generation of multimodal responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology*
  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • Cats
  • Evoked Potentials, Auditory / drug effects
  • Evoked Potentials, Auditory / physiology
  • Evoked Potentials, Somatosensory / drug effects
  • Evoked Potentials, Somatosensory / physiology
  • Evoked Potentials, Visual / drug effects
  • Evoked Potentials, Visual / physiology
  • Excitatory Amino Acid Antagonists / pharmacology*
  • Female
  • Mental Processes / drug effects
  • Mental Processes / physiology*
  • Neurons, Afferent / drug effects*
  • Receptors, AMPA / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / physiology*
  • Superior Colliculi / cytology
  • Superior Colliculi / drug effects
  • Superior Colliculi / physiology*

Substances

  • Excitatory Amino Acid Antagonists
  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • 2-Amino-5-phosphonovalerate