Commissural Excitation and Inhibition by the Superior Colliculus in Tectoreticular Neurons Projecting to Omnipause Neuron and Inhibitory Burst Neuron Regions

Abstract

Previous electrophysiological studies have shown that the commissural connections between the two superior colliculi are mainly inhibitory with fewer excitatory connections. However, the functional roles of the commissural connections are not well understood, so we sought to clarify the physiology of tectal commissural excitation and inhibition of tectoreticular neurons (TRNs) in the "fixation " and "saccade " zones of the superior colliculus (SC). By recording intracellular potentials, we identified TRNs by their antidromic responses to stimulation of the omnipause neuron (OPN) and inhibitory burst neuron (IBN) regions and analyzed the effects of stimulation of the contralateral SC on these TRNs in anesthetized cats. TRNs in the caudal SC (saccade neurons) projected to the IBN region, and received mono- or disynaptic inhibition from the entire rostrocaudal extent of the contralateral SC. In contrast, TRNs in the rostral SC projected to the OPN or IBN region and received monosynaptic excitation from the most rostral level of the contralateral SC, and mono- or disynaptic inhibition from its entire rostrocaudal extent. Among the rostral TRNs with commissural excitation, IBN-projecting TRNs also projected to Forel's field H (vertical gaze center), suggesting that they were most likely saccade neurons related to vertical saccades. In contrast, TRNs projecting only to the OPN region were most likely fixation neurons. Most putative inhibitory neurons in the rostral SC had multiple axon branches throughout the rostrocaudal extent of the contralateral SC, whereas excitatory commissural neurons, most of which were rostral TRNs, distributed terminals to a discrete region in the rostral SC.

Control of the superior colliculus by the lateral prefrontal cortex

“…This visual discharge is accompanied by a suppression of activity of saccade-related neurons in the SC on the opposite side of the brain. This push -pull relationship between activity in the left and right SCs is mediated by intercollicular inhibition [33,34], and prevents simultaneous programming of incompatible saccades. On prosaccade trials, this visual response was followed closely by a burst of activity beginning just prior to generation of the saccade into the neuron's response field.…”

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

“…The experimental arrangements for electrophysiological studies were the same as those described in detail previously (Takahashi et al 2005a(Takahashi et al , 2007. Briefly, the parietal and occipital cortex over the SC was removed bilaterally by aspiration to allow the introduction of stimulating electrodes into the right SC and a recording electrode into the left SC under direct visual observation.…”

“…TRNs receive excitatory and inhibitory inputs from many areas, such as the visual association cortex, the frontal eye field, substantia nigra pars reticulata, and the cerebellum. Commissural inputs from the opposite SC are also important sources of input to TRNs (Maeda et al 1979;May 2006;Mize 1992;Moschovakis et al 1988;Olivier et al 1998;Takahashi et al 2005aTakahashi et al , 2007.…”

“…However, recent electrophysiological studies have shown that a strong excitatory connection exists between the SCs, in addition to commissural inhibition. Furthermore, they showed that excitatory commissural effects were restricted to TRNs in the rostral SC, whereas inhibitory commissural effects extended to TRNs in the entire rostrocaudal extent of the SC (Munoz and Istvan 1998;Takahashi et al 2005a). More specifically, a mirror symmetric-like distribution of the excitatory commissural connection was found to connect the medial to medial and lateral to lateral parts of the two SCs, whereas the inhibitory commissural connection was present between the medial part of one SC and the lateral part of the other SC (Takahashi et al 2007).…”

Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity

“…The rostrocaudal spatial distribution of activity was obtained by including the 45 cells we recorded on the motor map (18 in the 53°zone, 21 in 13°zone and 6 between the zones) plus the 17 SCFNs described by Choi and Guitton (2006). We included SCFNs because (1) a number of studies have suggested that there is no discontinuity between the very rostral and remaining SC map Keller, 1997, 1999;Anderson et al, 1998;Krauzlis, 2005;Hafed et al, 2009), such that inclusion of SCFNs in the spatiotemporal evolution of activity provides a complete picture of map activity and (2) the very rostral SC and the remaining motor map are anatomically linked (Munoz and Istvan, 1998;Takahashi et al, 2005). However, since SCFNs were essentially silent (Choi and Guitton, 2006) until ϳ50 -80 ms after gaze shift end (Fig.…”