Topographic Organization of Excitatory and Inhibitory Commissural Connections in the Superior Colliculi and Their Functional Roles in Saccade Generation

Abstract

Takahashi M, Sugiuchi Y, Shinoda Y. Topographic organization of excitatory and inhibitory commissural connections in the superior colliculi and their functional roles in saccade generation. J Neurophysiol 104: 3146 -3167, 2010. First published October 6, 2010 doi:10.1152/jn.00554.2010. Our electrophysiological study showed that there are topographic connections between excitatory and inhibitory commissural neurons (CNs) in one superior colliculus (SC) and tectoreticular neurons (TRNs) in the opposite SC. To obtain morphological evidence for these topographic commissural connections between the SCs, tracers were injected into various parts of the SC, the inhibitory burst neuron (IBN) area and Forel's field H (FFH), in the cat. Retrogradely labeled CNs were classified into three types according to their somatic areas and identified as GABA-positive or -negative immunohistochemically. Caudal SC injections labeled small GABA-positive CNs (Ͻ200 m 2 ) in the deep layers of the opposite rostral SC. Rostral SC injections mainly labeled medium-sized GABA-negative CNs (200 -700 m 2 ) in the upper intermediate layer of the opposite rostral SC and small GABA-positive CNs in its deeper layers. Lateral SC injections labeled small GABA-positive CNs in the opposite medial SC and mainly medium-sized GABA-negative CNs in its lateral part. Medial SC injections labeled small GABA-positive CNs in the lateral SC and medium-sized GABA-negative CNs in the medial SC. In comparison, TRNs projecting to the FFH or IBN region were large (Ͼ700 m 2 ) and medium-sized. Many of the mediumsized GABA-negative CNs were TRNs projecting to the FFH. These results indicate that mirror-symmetric excitatory pathways link medial to medial (upper field) and lateral to lateral (lower field) parts of the SCs, whereas upper and lower field representations are linked by reciprocal inhibitory pathways in the tectal commissure. These connections presumably play important roles in conjugate upward and downward vertical saccades.

Greater benefits of multisensory integration during complex sensorimotor transformations

“…Although such activation is weak (after all, errors occur on only approximately 20% of all tactile trials), its initial oculomotor representation (e.g., within the SC) enables interactions with the oculomotor representation of the visual stimulus. Theoretical and experimental studies have suggested that interactions within the SC are governed by topographically dependent mechanisms enforcing local excitation and distal inhibition (Arai and Keller 2005;Dorris et al 2007;Grossberg et al 1997;Marino et al 2011;McPeek and Keller 2002;Meredith and Ramoa 1998;Munoz and Istvan 1998;Sooksawate et al 2011;Takahashi et al 2010), potentially by mechanisms of divisive normalization across the population (Ohshiro et al 2011). We speculate that weak activation of opposing SC shortly after presentation of visuotactile stimuli in the crossed posture leads to mutual inhibition via the spatial principle (Fig.…”

Visual Fixation as Equilibrium: Evidence from Superior Colliculus Inactivation

“…These correlated changes suggest that the involvement of the dSC in the triggering and dynamics of saccades rest upon shared processes (see also Figures 3C and 5A in Sparks et al (1990) as well as Stanford et al (1996) for comparable observations using electrical microstimulation techniques). The changes that affect contralesional saccades likely result from a diffusion of muscimol toward the site encoding the tested peripheral target (see Methods) whereas those altering ipsilesional saccades could result from disinhibition of neurons in the opposite dSC via inhibitory inter-collicular connections (Takahashi et al, 2010). …”

Alterations to multisensory and unisensory integration by stimulus competition

“…GABA-ergic projection via the intercollicular commissure (Appell and Behan 1990;Munoz and Istvan 1998;Sooksawate et al 2011;Takahashi et al 2010). Likewise, recent studies have demonstrated that the substantia nigra pars reticulata (SNr), in addition to its well-known inhibitory projection to the ipsilateral SC (Chevalier et al 1984;Hikosaka and Wurtz 1983;Karabelas and Moschovakis 1985;May and Hall 1984), provides a crossed inhibitory input to the opposite SC Liu and Basso 2008).…”