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

Abstract

The onset and vector of orienting behaviors, such as saccades, are controlled by commands that descend from a population of neurons in deep layers of the superior colliculus (dSC). In this study, to characterize the role of the collicular local circuitry that generates the spatiotemporal pattern of command activity in the dSC neuronal population, responses evoked by single-pulse electrical stimulation in superficial layers of the superior colliculus (sSC) were analyzed by a 64-channel field potential recording system (planar electrode, 8 ϫ 8 pattern; 150 m interelectrode spacing) in slices obtained from 16-to 22-d-old mice. A negative field potential with short latency and short duration spatially restricted to the recording sites in sSC was evoked adjacent to the stimulation site. After bath application of 10 M bicuculline, the same stimulus induced a large negative field response with long duration that spread from sSC to dSC. The dSC potential initially showed a positive response, presumably because of reversal of the negative potential that originated in sSC, and then a long negative response that spread horizontally as far as 1 mm. These responses disappeared after application of an NMDA receptor antagonist, 2-amino-5-phosphonovelarate, indicating that NMDA receptors have an important role in the generation of these responses. Simultaneous whole-cell patch-clamp recordings showed that the long-lasting negative field potentials corresponded to the depolarization accompanying burst spike activity of SC neurons. The present study revealed an extensive excitatory network in the dSC that may contribute to the generation of activity by a large population of neurons that discharge before a saccade.

Intralaminar and Interlaminar Activity within the Rodent Superior Colliculus Visualized with Voltage Imaging

“…The faint blue regions in the SGI and deep layers (Fig. 12 C,G ) indicate that GABA A receptors ordinarily limit the spread of activity into this region, consistent with recent reports (Saito and Isa, 2003; Phongphanphanee et al, 2008; Isa and Hall, 2009). Quantitative analyses of drug effects on mediolateral and dorsoventral spread are described in detail below (Figs.…”

S-ketamine influences strategic allocation of attention but not exogenous capture of attention

“…In addition, s-ketamine also blocks NMDA receptors within the Superior Colliculi of the mid-brain (SC; cf. Dumanskaya, Kosheleva, & Veselovsky, 2012;Phongphanphanee, Kaneda, & Isa, 2008; see also Grossberg, Roberts, http Aguilar, & Bullock, 1997). The SC also play an active role in shifting visual attention, steering saccades, and inhibiting of attention shifts back to a previously attended (or cued) position (Dorris, Klein, Everling, & Munoz, 2002;Everling, Dorris, Klein, & Munoz, 1999;Fecteau, Bell, & Munoz, 2004;Sapir, Soroker, Berger, & Henik, 2001).…”

Spatiotemporal analysis of electrically evoked activity in the chicken optic tectum: a VSDI study

“…In the SC of the rat, Binns and Salt (1997) showed that GABA reduces responses of superficial gray neurons to visual stimuli and is important for surround inhibition in vivo. In vitro, disinhibition enhanced response amplitudes in the avian TeO (Dye and Karten 1996) or the SC (Özen et al 2000;Phongphanphanee et al 2008;Saito and Isa 2003;Vokoun et al 2010) and increased the active area (Phongphanphanee et al 2008;Vokoun et al 2010).…”

“…Previous in vitro work has shown that neuronal responses in the TeO and the SC are highly regulated by GABA release. Disinhibition by GABA A receptor blockers usually enhanced signal amplitudes in whole cell or extracellular recordings (Dye and Karten 1996; Özen et al 2000;Phongphanphanee et al 2008;Saito and Isa 2003) and in optical imaging recordings of the SC (Vokoun et al 2010). In the SC, it also altered the spatial distribution (Phongphanphanee et al 2008;Vokoun et al 2010).…”

“…Recent work in other vertebrate tecta and in the mammalian SC addressed this issue by using electrode arrays or voltagesensitive dye imaging (VSDI) (Isa and Hall 2009;Kinoshita et al 2002;Phongphanphanee et al 2008;Vokoun et al 2010). Compared with the SC, the avian TeO has experimental advantages such as a distinct lamination and clearly separated input and output layers (Kanaseki and Sprague 1974;Luksch 2003), whereas the overall functional architecture appears to be matchable (Luksch 2009).…”