The superficial grey layer of the superior colliculus (SGS) contains a high proportion of GABAergic inhibitory neurones. We have investigated the role of GABA receptors in synaptic transmission of aspects of visual activity in the SGS that may be driven by inhibitory mechanisms, such as surround inhibition and response habituation.
Multi‐barrel glass iontophoretic pipettes were used to record single neuronal activity in the SGS of urethane‐anaesthetized rats. Visual stimulation was provided by the display of moving bars and stationary spots of light on a monitor placed in the receptive field.
Both ejection of GABA and the GABAB agonist baclofen reduced responses to moving bars (interstimulus intervals ≥ 8 s). The effects of GABA were reversed by the GABAA antagonist bicuculline, and the effects of baclofen were antagonized by the GABAB antagonist CGP 35348.
Surround inhibition was estimated by plotting the response to flashed spots of increasing diameter. In controls, expanding the spot diameter beyond the excitatory receptive field caused a decrease in the response. This inhibitory surround was reversibly reduced by bicuculline, but CGP 35348 had no effect.
Response habituation is the progressive reduction in the visual response during repetitive stimulus presentation. In controls, the visual response was reduced to 44 ± 3% of its initial level when a stimulus (moving bar) was presented 5 times with an interstimulus interval of 0.5 s. During CGP 35348 ejection, response habituation was reversibly reduced. Bicuculline had no effect on response habituation.
The effects of bicuculline on surround inhibition in the superior colliculus are consistent with similar studies in the lateral geniculate nucleus which indicate that GABAA receptors mediate this effect. The function of GABAB receptors in the visual system is less well researched. The reduction of response habituation with CGP 35348 demonstrates that, at least in the SGS, GABAB receptors have an important role in visual transmission which is distinct from that of GABAA receptors.
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.
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