Organization of Interlaminar Interactions in the Rat Superior Colliculus

Abstract

. Our previous studies have shown that when slices of the rat superior colliculus (SC) are exposed to a solution containing 10 M bicuculline and a low concentration of Mg 2ϩ (0.1 mM), most neurons in the intermediate gray layer (stratum griseum intermediale; SGI), wide-field vertical (WFV) cells in the optic layer (stratum opticum; SO), and a minor population of neurons in the superficial gray layer (stratum griseum superficiale; SGS) exhibit spontaneous depolarization and burst firing, which are synchronous among adjacent neurons. These spontaneous and synchronous depolarizations were thought to share common mechanisms with presaccadic burst activity in SGI neurons. In the present study, we explored the site responsible for generation of synchronous depolarization of SGI neurons by performing dual whole cell recordings under different slice conditions. A pair of SGI neurons recorded in a small rectangular piece of the SGI punched out from the SC slice showed synchronous depolarization but far less frequently than those recorded in a small rectangular piece including SGS and SO. This suggests that the superficial layers are needed for triggering synchronous depolarization in the SGI. Furthermore, we recorded spontaneous depolarizations in pairs of neurons belonging to the different layers. Analysis of their synchronicity revealed that WFV cells in the SO exhibit synchronous depolarizations with both SGS and SGI neurons, and the onset of spontaneous depolarization in WFV cells precedes those of neurons in other layers. Further, when SGS and SGI neurons exhibit synchronous depolarizations, SGI neurons usually precede the SGS neurons. These observations give further evidence to the existence of interlaminar interaction between superficial and deeper layers of the SC. In addition, it is suggested that WFV cells can trigger burst activity in other layers of the SC and that there is an excitatory signal transmission from the deeper layers to the superficial layers. I N T R O D U C T I O NOrienting behaviors such as saccades are preceded by burst firing of neurons in the deeper layers (intermediate and deep layers) of the mammalian superior colliculus (SC). The burst activity determines both the metrics and timing of saccades (Munoz and Wurtz 1995;Schiller and Koerner 1971;Schiller and Stryker 1972; Sparks and May 1980;Sparks et al. 1976;Wurtz and Goldberg 1972). Previous studies have suggested that the burst activity is attributed to local excitatory interactions by recurrent collaterals of deep layer neurons (Bozis and Moschovakis 1998; Moschovakis et al. 1988a,b).In our previous studies, using whole cell patch-clamp technique in rat brain stem slice preparations, we demonstrated the presence of local excitatory interactions among a large number of SGI neurons that communicate through excitatory recurrent connections (Isa et al. 1998; Isa 2003, 2004). Recruitment of these neurons to excitatory interactions was dependent on both activation of N-methyl D-aspartate (NMDA) receptors and release from GABAergic inhibition...

A population of gap junction-coupled neurons drives recurrent network activity in a developing visual circuit

“…Local recurrent network activity has been described in many areas of other vertebrate central nervous systems, including the SC Isa 2003, 2005), where it was found that, similar to what we observe in the optic tectum, the neurons of the stratum griseum intermediale receive strong synchronous excitatory drive from the more superficial layers (Saito and Isa 2005). Could it be that the synchronous nature of this local excitatory input from the more superficial layers of the SC could be due to the presence of gap junction coupling?…”

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

“…With the use of juxtacellular labeling, we revealed that the ON + Pause + OFF responses were observed in a variety of morphological types of sSC neurons. These include WFV and NFV cells, which are reported to be excitatory neurons (Isa et al, 1998;Saito and Isa, 2005;Kaneda et al, 2008), and stellate, piriform, multipolar, and horizontal cells that are considered to be inhibitory GABAergic neurons (Mize, 1992;Endo et al, 2003;Kaneda et al, 2008). Three marginal cells, which are projection neurons (Mooney et al, 1988) and have not been characterized as GABAergic (Mize, 1992), also exhibited the ON + Pause + OFF responses.…”

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

“…This approach reveals that the circuitry involved in transforming visual signals into eye movement commands can be preserved within a 300–400 μ m slice (Özen et al, 2000; Saito and Isa, 2005; Lee and Hall, 2006). Furthermore, these works suggest that the membrane properties of individual neurons are inadequate to account for specific aspects of their discharge properties, notably the robust bursting of SC output neurons.…”