Inhibition of superior colliculus neurons by a GABAergic input from the pretectal nuclear complex in the rat

Abstract

The mammalian pretectal nuclear complex (PNC) is a visual and visuomotor control structure which is strongly connected to other subcortical visual structures. This indicates that the PNC also controls subcortical visual information flow during the execution of various oculomotor programs. A prominent, presumably GABAergic, projection from the PNC targets the superficial grey layer of the superior colliculus (SC), which itself is a central structure for visual information processing necessary for the generation of saccadic eye movements. In order to characterize the pretectotectal projection in vitro, we performed whole-cell patch-clamp recordings from SC and PNC neurons in slices obtained from 3-6-week-old pigmented rats. Focal glutamate injections into the PNC and electrical PNC stimulation were used to induce postsynaptic responses in SC neurons. Electrical stimulation of the SC allowed electrophysiological identification of PNC neurons that provide the inhibitory pretectotectal input. Only inhibitory postsynaptic currents could be elicited in SC neurons both by pharmacological and by electrical activation of the ipsilateral PNC. Concomitantly, a small number of PNC neurons could be antidromically activated from the ipsilateral SC. Most SC cells postsynaptic to the prectectal input showed the dendritic morphology of wide-field and narrow-field cells and are therefore regarded as projection neurons. All inhibitory currents evoked by PNC activation could be completely blocked by bath application of the selective GABA(A) receptor antagonist bicuculline. Together these results indicate that SC projection neurons receive a direct inhibitory input from the ipsilateral PNC and that this input is mediated by GABA(A) receptors.

GABAergic pathways in the rat subcortical visual system: a comparative study in vivo and in vitro

“…For the pretecto‐tectal pathway, evidence indicates that most (80%) of the target neurones in the stratum griseum superficiale (SGS) are projection neurones (Baldauf et al. , 2003; Born & Schmidt, 2004), whereas for the pretecto‐geniculate pathway local GABAergic interneurones receive most of the pretectal input (Cucchiaro et al. , 1991; Wahle et al.…”

“…In order to verify that we also activated these projections by electrical stimulation, we identified antidromic activation of PNC neurones after stimulation in the dLGN. In a previous study, we used this method to verify results from the orthodromic stimulation of the pretecto‐tectal projection (Born & Schmidt, 2004). In response to electrical dLGN stimulation, we expected to record action potentials in PNC neurones, which appear at a constant latency and which persist in the presence of CNQX and kynurenic acid.…”

“…Furthermore, orthodromic electrical activation of PNC fibres evoked IPSCs that were insensitive to the glutamate receptor antagonists CNQX and kynurenic acid but could be blocked by bath application of bicuculline, a selective GABA A receptor antagonist. Similar results were reported previously for the pretecto‐tectal projection (Born & Schmidt, 2004). Thus, the pathways to both the dLGN and SC are GABAergic, as was proposed earlier based on anatomical criteria (Cucchiaro et al.…”

Whole-Brain Activity Maps Reveal Stereotyped, Distributed Networks for Visuomotor Behavior

“…In particular, responses to rotational motion stimuli were strongly suppressed. While we are not aware of previous functional evidence for such neurons integrating binocular visual information in the tectum, anatomical tracing experiments have identified bilateral projections in mammals from the pretectum to the superior colliculus, the optic tectum homolog, and in vitro recordings have confirmed functional inhibitory connections (Baldauf et al, 2003; Born and Schmidt, 2004). The preference for NT motion suggests that they would respond strongly to re-afferent motion signals during forward locomotion, and could be involved in gating visual processing, or detecting the proximity of objects, during swimming.…”

Modulation of GABAergic inhibition in the rat superior colliculus by a presynaptic group II metabotropic glutamate receptor

“…The three classes of GABA receptor are also relatively abundant and each plays distinct roles in collicular neuronal processing (Binns & Salt, 1997;Schmidt et al 2001). The SC also receives GABAergic input from the substantia nigra, zona incerta, pretectum and the contralateral colliculus (Mize, 1992;Baldauf et al 2003;Born & Schmidt, 2004). The variability of the IPSC paired-pulse behaviour under control conditions (prior to Group II agonist application) is consistent with the notion that there is a substantial variation of inhibitory circuits, but it is nevertheless noteworthy that in all cases IPSCs were affected in the same way by Group II receptor activation.…”