Cellular morphology in the visual layer of the developing rat superior colliculus

Labriola, Anna R.; Laemle, Lois K.

doi:10.1016/0014-4886(77)90174-1

Cited by 43 publications

(31 citation statements)

References 21 publications

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“…We found that the dendritic arbors of neurons in the SGS of the SC were dramatically more complex during the first postnatal week than one would expect based on previous studies in the rat (Labriola and Laemle 1977;Tenório et al 1996;Warton and Jones 1985). Species differences between mice and rats are unlikely to account for such a substantial difference in dendritic complexity, but other methodological differences may be important.…”

Section: Discussioncontrasting

confidence: 54%

“…We examined the morphological properties of some of the recorded neurons by including an Alexa dye in the whole cell recording solution and then reconstructing their morphology off-line (see MATERIALS AND METHODS). Surprisingly in view of previous Golgi studies of the SC (Labriola and Laemle 1977;Tenório et al 1996;Warton and Jones 1985), most neurons in our study exhibited complex dendritic morphology, including secondary and tertiary branches, as early as P3-4 (Fig. 7).…”

Section: Resultsmentioning

confidence: 83%

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Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening

Furman

Crair

2012

Journal of Neurophysiology

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In the developing visual system of mammals, retinal axons from the two eyes compete for postsynaptic partners. After eye opening, this process is regulated in part by homeostatically constrained competition for synaptic connectivity with target neurons. However, prior to eye opening, the functional and synaptic basis of binocular map development is unclear. To examine the role of binocular interactions during early stages of visual map development, we performed in vitro patch-clamp recordings from the superior colliculus (SC) of neonatal mice. Using newly designed slice preparations, we compared retinocollicular synapse development in the medial SC, which receives binocular input, and the lateral SC, which is predominantly monocular. Surprisingly, we found that at P6-7, when eye-specific segregation has just emerged, retinocollicular synapses were stronger and more mature and dendritic arbors were more elaborate in the medial than the lateral SC. Furthermore, monocular enucleation of the ipsilateral eye at P0 selectively reduced synaptic strength and dendritic branching in the medial SC and abolished the differences normally observed between the two slices at P6-7. This specifically implicates binocular interactions in the development of retinocollicular connectivity prior to eye opening. Our findings contrast with the predictions of a constrained-connectivity model of binocular map development and suggest instead that binocular competition prior to eye opening enhances retinocollicular synaptic strength and the morphological development of retino-recipient neurons.

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Section: Discussioncontrasting

confidence: 54%

Section: Resultsmentioning

confidence: 83%

Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening

Furman

Crair

2012

Journal of Neurophysiology

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“…8). We concentrated on the morphologies of the cells in the superficial SC layers, because these have been described in detail (e.g., Langer and Lund, 1974;Labriola and Laemle, 1977;Wharton and Jones, 1985). The CaBP-labeled material contained examples of all of the major cell types described in Golgi-stained sections (Langer and Lund, 1974;Labriola and Laemle, 1977).…”

Section: Fig 6 Histograms Showing the Percent Frequency Of Calbindimentioning

confidence: 99%

CalbindinD28k- and parvalbumin-immunoreactive neurons form complementary sublaminae in the rat superior colliculus

1998

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By using light microscopic immunocytochemistry and computer analysis, we have mapped the distributions of two calcium-binding proteins (CaBPs), calbindinD28k (CB) and parvalbumin (PV), in the rat superior colliculus (SC). The patterns of CaBP expression were complementary. A band of heavily labeled, medium-sized CB-immunoreactive cells (CB-cells) was centered in the optic layer (OL), whereas PV-immunoreactive cells (PV-cells) were found predominantly in the intermediate gray layer (IGL), where they were clustered within patches of PV-labeled fibers. The superficial gray layer (SGL) could be divided into two sublaminae. CB-cells were found mostly in the dorsal half of the SGL, whereas PV-cells were scattered throughout the ventral SGL and the dorsal OL. Most of the CaBP-immunoreactive cells in the SGL were small bipolar cells with vertically oriented dendrites; however, there were also some PV-cells with horizontally oriented dendrites. Quantitative analysis of the CaBP distributions reinforced our observations that these cells are distributed in complementary tiers that are not restricted to the traditional laminae. The size and shape of some of these tiers were determined from a three-dimensional reconstruction of serial sections. The complementarity of the CaBP-immunoreactive tiers was also confirmed by fluorescence microscopy of double-labeled sections, in which few if any double-labeled neurons were observed. Complementary tiers of CB-cells and PV-cells have been observed previously in the SC of the cat. The present results demonstrate them in another species and further suggest that there are functional sublaminae in the SC that can be distinguished by CaBP content.

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“…We could not recover or had to discard morphological data for the remaining 21 neurons because labeling was not observed in 6 cases, it was too faint to trace dendritic arbors in 5 cases, or 2 or more neurons were labeled in 10 cases (although only 1 neuron was targeted in each of those recordings). Based on the location of soma and somatodendritic morphologies (Langer and Lund, 1974; Tokunaga and 15 Otani, 1976;Labriola and Laemle, 1977;Mooney et al, 1985Mooney et al, , 1988Edwards et al, 2002), we classified the labeled neurons into 7 types ( Fig. 2A), including wide-field vertical (WFV; n = 4; Fig.…”

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

Kaneda

Isa

2013

Neuroscience

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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...

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Cellular morphology in the visual layer of the developing rat superior colliculus

Cited by 43 publications

References 21 publications

Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening

Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening

CalbindinD28k- and parvalbumin-immunoreactive neurons form complementary sublaminae in the rat superior colliculus

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

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