SGI Neurons Research Articles

Development of a neural circuit in the superior colliculus

The superior colliculus is important for orientation behaviors, in which visuomotor transformation is performed by the pathway from the superficial layer (SGS) to the intermediate layers (SGI). The opposite pathway (from the SGI to the SGS) also exists, raising the possibility of a feedback circuit, although it could be either negative (inhibitory) or positive (excitatory). In this study, we focused on the development of the feedback circuit. We used optical imaging methods that can measure neuronal population responses directly, as the orientation behaviors are determined by large population activities of superior colliculus neurons. We examined the postnatal development of the propagation pattern of neuronal excitation from the SGI to the SGS using a GABAA receptor antagonist. The optical response propagated within the SGI, but not to the SGS in infant mice that have not opened their eyes. In contrast, in young mice after eye opening, the optical response propagated initially in the SGI and then to the SGS. The GABAA receptor antagonist increased the optical response in the SGS in young mice, as well as that in the SGI in infant mice. Together, these results suggest that axons of SGI neurons terminate to the SGS during development after eye opening.

Cholinergic responses in GABAergic and non‐GABAergic neurons in the intermediate gray layer of mouse superior colliculus

Neurons in the intermediate gray layer (SGI) of the mammalian superior colliculus (SC) receive dense cholinergic innervations from the brainstem parabrachial region. Such cholinergic inputs may influence execution of orienting behaviors. To obtain deeper insights into how the cholinergic inputs modulate the SC local circuits, we analysed the cholinergic responses in identified γ-aminobutyric acid (GABA)ergic and non-GABAergic neurons using SC slices obtained from GAD67-GFP knock-in mice. The responses of SGI neurons to cholinergic agonists were various combinations of fast inward currents mediated mainly via α4β2 and partly by α7 nicotinic receptors (nIN), slow inward currents caused by activation of M1 plus M3 muscarinic receptors (mIN), and slow outward currents caused by activation of M2 muscarinic receptors (mOUT). The most common cholinergic responses in non-GABAergic neurons was nIN + mIN + mOUT (38/68), followed by nIN + mIN (16/68), nIN + mOUT (11/68), nIN only (2/68), and no response (1/68). On the other hand, the major response pattern in GABAergic neurons was either nIN only (26/54) or nIN + mIN (21/54), followed by nIN + mOUT (4/54), mOUT only (2/54), and no response (1/54). Thus, major effects of cholinergic inputs to both SGI GABAergic and non-GABAergic neurons are excitatory, but the response patterns in these two types of SGI neurons are different. Thus, actions of the cholinergic inputs to non-GABAergic and GABAergic SGI neurons are not simple push-pull mechanisms, like excitation vs inhibition, but might cooperate to balance the level of excitation and inhibition for setting the state of the response property of the local circuit.

A Circuit Model for Saccadic Suppression in the Superior Colliculus

Attenuation of visual activity in the superficial layers (SLs), stratum griseum superficiale and stratum opticum, of the superior colliculus during saccades may contribute to reducing perceptual blur during saccades and also may help prevent subsequent unwanted saccades. GABAergic neurons in the intermediate, premotor, layer (SGI), stratum griseum intermedium, send an inhibitory input to SL. This pathway provided the basis for a model proposing that the SGI premotor cells that project to brainstem gaze centers and discharge before saccades also activate neighboring GABAergic neurons that suppress saccade-induced visual activity in SL. The in vitro method allowed us to test this model. We made whole-cell patch-clamp recordings in collicular slices from either rats or GAD67-GFP knock-in mice, in which GABAergic neurons could be identified by their expression of green fluorescence protein (GFP). Antidromic electrical stimulation of SGI premotor cells was produced by applying pulse currents in which their axons congregate after exiting the superior colliculus. The stimulation evoked monosynaptic EPSCs in SGI GABAergic neurons that project to SL, as would be predicted if these neurons receive excitatory input from the premotor cells. Second, IPSCs were evoked in SL neurons, some of which project to the visual thalamus. These IPSCs were polysynaptically mediated by the GABAergic neurons that were excited by the antidromically activated SGI neurons. These results support the hypothesis that collaterals of premotor neuron axons excite GABAergic neurons that inhibit SL visuosensory cells.

Identity of a pathway for saccadic suppression

Neurons in the superficial gray layer (SGS) of the superior colliculus receive visual input and excite intermediate layer (SGI) neurons that play a critical role in initiating rapid orienting movements of the eyes, called saccades. In the present study, two types of experiments demonstrate that a population of SGI neurons gives rise to a reciprocal pathway that inhibits neurons in SGS. First, in GAD67-GFP knockin mice, GABAergic SGI neurons that expressed GFP fluorescence were injected with the tracer biocytin to reveal their axonal projections. Axons arising from GFP-positive neurons in SGI terminated densely in SGS. Next, SGI neurons in rats and mice were stimulated by using the photolysis of caged glutamate, and in vitro whole-cell patch-clamp recordings were used to measure the responses evoked in SGS cells. Large, synaptically mediated outward currents were evoked in SGS neurons. These currents were blocked by gabazine, confirming that they were GABA(A) receptor-mediated inhibitory postsynaptic currents. This inhibitory pathway from SGI transiently suppresses visual activity in SGS, which in turn could have multiple effects. These effects could include reduction of perceptual blurring during saccades as well as prevention of eye movements that might be spuriously triggered by the sweep of the visual field across the retina.

Organization of Interlaminar Interactions in the Rat Superior Colliculus

Our previous studies have shown that when slices of the rat superior colliculus (SC) are exposed to a solution containing 10 microM bicuculline and a low concentration of Mg2+ (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.

Projections from the rostral pole of the inferior colliculus to the cat superior colliculus

The neuroanatomical data given here reveal a dense projection from the rostral pole of the cat inferior colliculus (rpIC) to the superior colliculus (SC). A portion of this pathway distributes in ‘patches’ across the ventral portion of the intermediate grey layer. These finding suggest that the rpIC input to the SC might play a role in determining the auditory receptive fields of SGI neurons and in the construction of the SC’s precise two dimensional map of auditory space.

Voltage-gated transient outward currents in neurons with different firing patterns in rat superior colliculus.

1. We investigated the electrophysiological properties of transient outward currents (TOCs) in neurons with different firing patterns, regular-spiking, fast-spiking and late-spiking neurons, in the intermediate layer (SGI) of the superior colliculus using the whole-cell patch clamp technique in slice preparations obtained from young rats (post-natal days 17-22). 2. Analysis of inactivation kinetics and normalized amplitude revealed that TOCs in regular-and fast-spiking neurons had fast inactivation kinetics (decay time constants (mean +/- s.e.m.) of 13.8 +/- 1.5 and 11.4 +/- 1.2 ms, respectively) and low current densities (36.6 +/- 3.3 and 32.1 +/- 4. 9 pA pF-1, respectively). TOCs in late-spiking neurons, on the other hand, displayed a wide range of both inactivation kinetics (36.7 +/- 2.4 ms, with a range from 11.3 to 147.8 ms) and current density (54. 0 +/- 2.9 pA pF-1, with a range from 9.8 to 131.2 pA pF-1). 3. In regular-, fast- and late-spiking neurons having TOCs with slow time constants (> 50 ms, class II late-spiking neurons), the TOCs were sensitive to 4-aminopyridine (4-AP), with IC50 values of 2.9, 2.4 and 1.2 mM, respectively. In late-spiking neurons having TOCs with fast decay time constants (< 30 ms, class I late-spiking neurons), the TOCs were composed of at least two 4-AP-sensitive components (IC50 values of 0.2 microM and 3.6 mM). 4. Class I late-spiking neurons displayed non-inactivating outward currents which were highly sensitive to 4-AP. They changed their firing patterns to the regular-spiking mode, not only in response to low concentrations of 4-AP (< 50 microM), but also in response to dendrotoxin (200 nM), suggesting that non-inactivating outward currents contribute to the late-spiking property. However, the components of TOCs which were highly sensitive to 4-AP were also sensitive to dendrotoxin. These results suggest that both or either of the two currents contribute to the late-spiking property of class I late-spiking neurons. 5. Although class II late-spiking neurons also displayed non-inactivating outward currents, the late-spiking property was not abolished by low concentrations of 4-AP and dendrotoxin. They changed to a regular firing pattern in response to a high concentration of 4-AP (5 mM), suggesting that TOCs contribute to late-spiking property of class II late-spiking neurons. 6. The results suggest that TOCs with different properties contribute to the different firing patterns of SGI neurons.

The Visuo-Motor Pathway in the Local Circuit of the Rat Superior Colliculus

Intrinsic circuit of the superior colliculus (SC), in particular the pathway from the optic tract (OT) to neurons in the intermediate layer (SGI), was investigated by whole-cell patch-clamp recording in slice preparations obtained from 17- to 24-d-old rats. Stimulation of the OT induced monosynaptic EPSPs in neurons in the superficial gray layer (SGS) and the optic layer (SO), and disynaptic or polysynaptic EPSPs in a majority of SGI neurons. Stimulation of the SGS induced monosynaptic or oligosynaptic EPSPs in the SGI neurons. Both the monosynaptic EPSPs induced in the SGS/SO neurons by stimulation of the OT and those induced in the SGI neurons by stimulation of the SGS were mediated by AMPA- and NMDA-type glutamate receptors. Thus, we have clarified the existence of the glutamatergic excitatory pathway from the OT to the SGI neurons via SGS and SO neurons. The EPSPs in the SGI neurons induced by stimulation of the OT or SGS were remarkably enhanced by bicuculline, suggesting that the signal transmission in this pathway is under strong suppression by the GABAergic system.

Cortical somatosensory and trigeminal inputs to the cat superior colliculus: light and electron microscopic analyses.

Two different axonal transport tracers were used in single animals to test the hypothesis that the expansive intermediate gray layer of the cat superior colliculus (stratum griseum intermediale, SGI) is composed of sensorimotor domains. The results show that two sensory pathways, the trigeminotectal and the corticotectal arising from the fourth somatosensory area, commingle in patches across the middle tier of the SGI. Furthermore, the data reveal that tectospinal cells are distributed within these patches. Taken together, these results show a commingling of functionally related afferents and a consistent spatial relationship between these afferents and tectospinal neurons. These relationships indicate that the SGI consists of domains that can be distinguished by their unique combinations of afferent and efferent connections. The ultrastructural characteristics and synaptic relationships of these somatosensory afferent pathways suggest that they have distinct roles within the sensorimotor domain of the SGI. The trigeminotectal terminals are relatively small, contain round vesicles and make asymmetrical synapses on small, presumably distal, dendrites. We submit that these trigeminal terminals bestow the basic receptive field properties upon SGI neurons. In contrast, the somatosensory corticotectal terminals are relatively large, contain round vesicles, make asymmetrical synapses, participate in triads, and are presynaptic to proximal dendrites. We suggest that these cortical terminals bestow integrative abilities on SGI neurons.