Comparison of the ultrastructure of cortical and retinal terminals in the rat superior colliculus

Boka, Kamran; Chomsung, Ranida; Li, Jianli; Bickford, Martha E.

doi:10.1002/ar.a.20359

Cited by 21 publications

(25 citation statements)

References 47 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The ultrastructure of V1 corticotectal terminals and their postsynaptic targets in the mouse are remarkably similar to those of our previous study of V1 corticotectal terminals in the rat (Boka et al, ). In both species, corticotectal terminals are restricted to the SGS and SO and are small terminals (mouse 0.38 ± 0.21 μm 2 ; rat 0.44 ± 0.27 μm 2 ) that contain densely packed round vesicles and contact small caliber dendrites (mouse 0.31 ± 0.21 μm 2 ; rat 0.51 ± 0.69 μm 2 ).…”

Section: Discussionsupporting

confidence: 88%

Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

Masterson

Zhou

Akers

et al. 2018

J of Comparative Neurology

View full text Add to dashboard Cite

The superior colliculus (SC) is a major site of sensorimotor integration in which sensory inputs are processed to initiate appropriate motor responses. Projections from the primary visual cortex (V1) to the SC have been shown to exert a substantial influence on visually induced behavior, including “freezing.” However, it is unclear how V1 corticotectal terminals affect SC circuits to mediate these effects. To investigate this, we used anatomical and optogenetic techniques to examine the synaptic properties of V1 corticotectal terminals. Electron microscopy revealed that V1 corticotectal terminals labeled by anterograde transport primarily synapse (93%) on dendrites that do not contain gamma aminobutyric acid (GABA). This preference was confirmed using optogenetic techniques to photoactivate V1 corticotectal terminals in slices of the SC maintained in vitro. In a mouse line in which GABAergic SC interneurons express green fluorescent protein (GFP), few GFP‐labeled cells (11%) responded to activation of corticotectal terminals. In contrast, 67% of non‐GABAergic cells responded to activation of V1 corticotectal terminals. Biocytin‐labeling of recorded neurons revealed that wide‐field vertical (WFV) and non‐WFV cells were activated by V1 corticotectal inputs. However, WFV cells were activated in the most uniform manner; 85% of these cells responded with excitatory postsynaptic potentials (EPSPs) that maintained stable amplitudes when activated with light trains at 1–20 Hz. In contrast, in the majority of non‐WFV cells, the amplitude of evoked EPSPs varied across trials. Our results suggest that V1 corticotectal projections may initiate freezing behavior via uniform activation of the WFV cells, which project to the pulvinar nucleus.

show abstract

Section: Discussionsupporting

confidence: 88%

Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

Masterson

Zhou

Akers

et al. 2018

J of Comparative Neurology

View full text Add to dashboard Cite

show abstract

“…This could be supported by the fact that both types of sSC neurons receive glutamatergic inputs from the retina and the V1 (Boka et al, 2006), as well as GABAergic inputs from local interneurons (Endo et al, 2005;Kaneda et al, 2008). Our juxtacellular labelings showed that half of the labeled cells were putative excitatory neurons (4 WFV, 2 NFV, and 3 marginal cells out of 18 labeled neurons, Fig.…”

supporting

confidence: 59%

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

Kaneda

Isa

2013

Neuroscience

View full text Add to dashboard Cite

An object that suddenly appears in the visual field should be quickly detected and responded to because it could be beneficial or harmful. The superficial layer of the superior colliculus (sSC) is a brain structure capable of such functions, as sSC neurons exhibit sharp transient spike discharges with short latency in response to the appearance of a visual stimulus.However, how transient activity is generated in the sSC is poorly understood. Here, we show that inhibitory inputs actively shape transient activity in the sSC. Juxtacellular recordings from anesthetized mice demonstrate that almost all types of sSC neurons, which were identified by post hoc histochemistry, show transient spike discharges, i.e., ON activity, immediately after visual stimulus onset. ON activity was followed by a pause before the visual stimulus was turned off. To determine whether the pause reflected the absence of excitatory drive or inhibitory conductance, we injected depolarizing currents juxtasomally, which enabled us to observe inhibition as decreased discharges. The pause was observed even under this condition, suggesting that inhibitory input caused the pause. We further found that local application of a mixture of gamma aminobutyric acid (GABA) A and GABA B receptor antagonists additively diminished the pause. These results indicate that GABAergic inputs produce transient ON responses by attenuating excitatory activity through the cooperative activation of GABA A and GABA B receptors, allowing sSC neurons to act as a saliency detector. Detecting an object that suddenly appears in the visual field is crucial for animals because their survival may depend on whether the object is beneficial or harmful. Transient, but not persistent, spike discharges in the sensory systems should encode the detection of the appearance. One of the candidate nuclei for this function is the superior colliculus (SC), a midbrain structure that is critical for visuomotor information processing (Sparks, 1986;Isa and Sparks, 2006). The superficial layer of the SC (sSC) receives visual inputs from the retina and the primary visual cortex (V1) in a retinotopically organized manner (Dräger and Hubel, 1976;May, 2006). sSC neurons exhibit transient spike discharges, called ON responses, immediately after the appearance of a visual stimulus (Schiller and Koerner, 1971; Cynader, 1972, 1975;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Dräger and Hubel, 1975;Rhoades and Chalupa, 1977;Marrocco and Li, 1977;Moors and Vendrik, 1979;Wang et al., 2010), implying that the sSC could detect the appearance of the object. Indeed, lesions or inactivation of the SC cause a detection deficit of visual stimuli (Butter et al., 1978;Overton and Dean, 1988;Fitzmaurice et al., 2003).The sSC consists of several cell types, including excitatory and inhibitory neurons (Mize, 1992;Endo et al., 2003Endo et al., , 2005May, 2006;Kaneda et al., 2008). Previous intracellular recording and labeling studies elucidated that some sSC neurons responded to moving or static visual stim...

show abstract

“…In addition, due to the close relationship of the GABA shunt and Krebs cycle, GABA is prone to be accumulated in the mitochondria, but this is again more prominent in cells that utilized GABA as a neurotransmitter (Gibson and Dianel 2007). Previous studies have used retinotectal or corticothalamic terminals known to be GABA negative to establish baseline values (Mize and Butler 1996; Patel and Bickford 1997; Boka et al 2006). Because we did not have that option, in that corticotectal terminals in SGI cannot be specified on ultrastructural grounds, we measured the gold particle density over myelin sheaths, which should not be GABA + , for use as a baseline.…”

Section: Discussionmentioning

confidence: 99%

“…The ultrastructure of axonal terminals in the SC has been studied in rat (Boka et al 2006), cat (Norita 1980; Behan et al 1987) and monkey (Mize et al 1991). Using cats, Norita (1980) divided the terminals in the neuropil of the deep SC into seven categories, based on the shape of their vesicles and their postsynaptic profiles.…”

Section: Discussionmentioning

confidence: 99%

The macaque midbrain reticular formation sends side-specific feedback to the superior colliculus

2009

View full text Add to dashboard Cite

The central mesencephalic reticular formation (cMRF) likely plays a role in gaze control, as cMRF neurons receive tectal input and provide a bilateral projection back to the superior colliculus (SC). We examined the important question of whether this feedback is excitatory or inhibitory. Biotinylated dextran amine (BDA) was injected into the cMRF of M. fascicularis monkeys to anterogradely label reticulotectal terminals and retrogradely label tectoreticular neurons. BDA labeled profiles in the ipsi- and contralateral intermediate gray layer (SGI) were examined electron microscopically. Postembedding GABA immunochemistry was used to identify putative inhibitory profiles. Nearly all (94.7%) of the ipsilateral BDA labeled terminals were GABA positive, but profiles postsynaptic to these labeled terminals were exclusively GABA negative. In addition, BDA labeled terminals were observed to contact BDA labeled dendrites, indicating the presence of a monosynaptic feedback loop connecting the cMRF and ipsilateral SC. In contrast, within the contralateral SGI, half of the BDA labeled terminals were GABA positive, while more than a third were GABA negative. All the postsynaptic profiles were GABA negative. These results indicate the cMRF provides inhibitory feedback to the ipsilateral side of the SC, but it has more complex effects on the contralateral side. The ipsilateral projection may help tune the “winner-take-all” mechanism that produces a unified saccade signal, while the contralateral projections may contribute to the coordination of activity between the two colliculi.

show abstract

Comparison of the ultrastructure of cortical and retinal terminals in the rat superior colliculus

Cited by 21 publications

References 47 publications

Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

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

The macaque midbrain reticular formation sends side-specific feedback to the superior colliculus

Contact Info

Product

Resources

About