Release from GABAA receptor-mediated inhibition unmasks interlaminar connection within superior colliculus in anesthetized adult rats

Abstract

The superior colliculus (SC) contains two major subdivisions, the superficial layers (sSC) and the deeper layers (dSC). sSC receives visual information from the retina and visual cortex, while dSC sends descending projections to the brainstem and spinal cord. It has not been clear whether and how sSC directly activates dSC, however recent studies in slice preparations reported that electrical stimulation of sSC induces burst firing in dSC neurons after application of bicuculline. In the present study, we tested whether sSC directly activates dSC in vivo. In isoflurane-anesthetized rats, electrical stimulation of the optic nerve (ON) induced negative field responses mainly in sSC, but not as much in dSC, under control conditions. However, after injection of bicuculline into dSC, ON stimulation induced long-lasting negative field responses in dSC. dSC neurons including the tectofugal neurons exhibited burst firing during the long-lasting negative field responses. The burst responses remained after ablation of the cerebral cortex ipsilateral to the SC recordings. These results suggest that retinal inputs induce burst responses in tectofugal neurons in dSC via subcortical pathways when the SC circuit is released from GABA(A) receptor-mediated inhibition. We propose that sSC is the main candidate for the source of the excitatory synaptic inputs to dSC among the subcortical regions.

Spatiotemporal Profiles of Field Potentials in Mouse Superior Colliculus Analyzed by Multichannel Recording

“…A previous study of anesthetized rats from our laboratory (Katsuta and Isa, 2003) showed that electrical stimulation of the optic fibers at 2 mA, which activated both Y and W fibers, induced negative field responses in the most dorsal part of the sSC, whereas a reversed positive potential was observed in the ventral part of the sSC and in the dSC. Such a current sink and source relationship might be derived from neurons with cell bodies in the ventral part of the sSC or in the dSC and dendritic arborizations in the dorsal part of the sSC that receive input from the optic tract.…”

“…The circuits that organize this activity have been studied in vitro in slice preparations (for review, see Isa and Saito, 2001;Grantyn et al, 1984;Lee et al, 1997Lee et al, , 2007Isa et al, 1998;Meredith and Ramoa, 1998;Lo and Mize, 2000;Schmidt et al, 2001;Isa, 2002;Isa and Sparks, 2006;Neale and Salt, 2006;Kaneda et al, 2008). Furthermore, profiles of field potential responses at different depths evoked by sSC stimulation were measured by single-electrode recordings in anesthetized rats (Katsuta and Isa, 2003) and monkeys (Nikitin and Isa, 2004). However, these studies were performed using whole-cell recordings from individual neurons or field recording in one plane; hence, the information about the spatial and temporal properties of the whole population of dSC cells remained indirect and limited Isa, 2004, 2005).…”

Short-Latency Visual Input to the Subthalamic Nucleus Is Provided by the Midbrain Superior Colliculus

“…Intracollicular injections of bicuculline (0.5 μl; 0.5 μl/min) were made with a 10 μl Hamilton syringe (Scientific Laboratory Supplies Ltd., Nottingham, UK) mounted on an infusion pump, connected to the needle by a length of plastic tubing. The experimental rationale in the present study was based on the important observation of Katsuta and Isa (2003) that local intra-collicular injections of bicuculline can reinstate visual sensitivity to the SC deep layers rendered insensitive by urethane anesthesia. (Note: Throughout the current article, we adhere to the convention of referring to all SC layers underlying the superficial layers as the ‘deep layers’).…”

The efference cascade, consciousness, and its self: naturalizing the first person pivot of action control

“…Suffice it to say that it involves massive inhibitory interactions, both intrinsic to the colliculus (Katsuta and Isa, 2003) and coming from outside in the form of powerful inhibitory projections from several sources, only one of which is the already mentioned nigral projection. They include the zona incerta, anterior and posterior pretectal nuclei, the periparabigeminal area, a “critical zone” of the pedunculopontine region, and indirectly, via collicular interneurons, the parabigeminal nucleus (Ficalora and Mize, 1989; Appell and Behan, 1990; Behan and Appell, 1992; May et al, 1997; Durmer and Rosenquist, 2001; Klop et al, 2006; Lee and Hall, 2006).…”