Compensatory and transneuronal plasticity after early collicular ablation

Abstract

Plasticity within the visual system was assessed in the quokka wallaby following unilateral superior collicular (SC) ablation at postnatal days (P) 8-10, prior to the arrival of retinal ganglion cell (RGC) axons. At maturity (P100), projections were traced from the eye opposite the ablation, and total RGC numbers were estimated for both eyes. Ablations were partial (28-89% of SC remaining) or complete (0-5% of SC remaining). Projections to the visual centers showed significant bilateral (P < 0.05) increases in absolute volume. Minor anomalous projections also formed within the deep, surviving non-retino-recipient layers of the ablated SC and via a small bundle of RGC axons recrossing the midline to innervate discrete patches in the SC contralateral to the lesion. Total absolute volume of projections did not differ between partial and complete ablations; moreover, values did not differ from normal (P > 0.05). Compared with normal, total RGC numbers were significantly (P < 0.05) reduced in the eye opposite the ablation but increased (P < 0.05) in the other eye. Consequently, the sum of the two RGC populations did not differ from normal (P > 0.05). As in rodents, the visual system in quokka compensates following injury by maintaining a set volume of arborization but does so by forming only minor anomalous projections. Furthermore, increased RGC numbers in the eye ipsilateral to the lesion indicate that compensation occurs transneuronally, thus maintaining total numbers of projecting neurons. The implication is that the visual system acts in concert following unilateral injury to maintain set values for RGC terminal arbors as well as their cell bodies.

In vivo retinotopic mapping of superior colliculus using manganese-enhanced magnetic resonance imaging

“…Whether the lower intensity in the brighter half of left SC than the control right SC was related to secondary degeneration (Levkovitch-Verbin et al, 2003) in both groups remained to be elucidated. The current in vivo MEMRI approach may help evaluate at high resolutions the mechanisms guiding the establishment of topographically ordered connections in the central nervous system (McLaughlin et al, 2003;Scicolone et al, 2009;O'Leary, 1991, 1992), the progressive changes in functional topology in diseases involving partial visual field loss, such as glaucoma, age-related macular degeneration, ischemic stroke and traumatic brain injury (Boucard et al, 2009;Chan et al, 2010;Duncan et al, 2007;Gupta et al, 2009;Holcombe et al, 2008;Sauve et al, 1998), and the effect of interventions on neuronal rewiring upon early retinal and SC lesions (Chandrasekaran et al, 2005;Dunlop et al, 2007;Finlay et al, 1979;Jeffery and Thompson, 1986;Simon et al, 1994;So, 1979), which could eventually lead to new diagnostic techniques and therapies.…”

“…In particular, the superficial layers of the SC receive visual information from the retina in a topological order (McLaughlin et al, 2003;Plas et al, 2005;Siminoff et al, 1966;Simon and O'Leary, 1991), whereby the retinal ganglion cell axons emanating from superior, inferior, nasal and temporal retina projected to the contralateral lateral, medial, caudal and rostral SC respectively in rodents (McLaughlin et al, 2003;Plas et al, 2005;Siminoff et al, 1966;Simon and O'Leary, 1991). Despite the increasing number of studies investigating the retinotopic projection in visual brain development and disorders (Chandrasekaran et al, 2005;Dunlop et al, 2007;Finlay et al, 1979;Haustead et al, 2008;Jeffery and Thompson, 1986;McLaughlin et al, 2003;O'Leary and McLaughlin, 2005;Scicolone et al, 2009;Simon and O'Leary, 1992;So, 1979), the majority of in vivo techniques on brain organization, such as electrophysiology and optical imaging, focus on the cortex (Issa et al, 2008;Kalatsky et al, 2005;Kim et al, 2006;Peterson et al, 1998). The precise topological projection in the subcortical structures remains difficult to assess in vivo, due to the low spatial resolution of electrophysiological techniques, the depth limitation from optical imaging, the small sizes of the subcortical nuclei, their deep locations, and their closeness to surrounding large pulsating vessels (Chen et al, 1999;Fortune and Hood, 2003).…”

IN VIVOMULTIPARAMETRIC MAGNETIC RESONANCE IMAGING AND SPECTROSCOPY OF RODENT VISUAL SYSTEM

“…In particular, the superficial layers of the SC receive visual information from the retina in a topological order [4,8,102,103], whereby the retinal ganglion cell axons emanating from superior, inferior, nasal and temporal retina projected to the contralateral lateral, medial, caudal and rostral SC respectively in rodents [4,8,102,103]. Despite the increasing number of studies investigating the retinotopic projection in visual brain development and disorders [6,76,92,[103][104][105][106][107][108][109], the majority of in vivo techniques on brain organization, such as electrophysiology and optical imaging, focus on the cortex [9,[110][111][112]. The precise topological projection in the subcortical structures remains difficult to assess in vivo, due to the low spatial resolution of electrophysiological techniques, the depth limitation from optical imaging, the small sizes of the subcortical nuclei, their deep locations, and their closeness to surrounding large pulsating vessels [113,114].…”

“…Future experiments may also test the feasibility of activity-induced MEMRI [133] to map retinotopic activities in the visual nuclei during brain development, diseases, plasticity and regeneration therapies at high resolutions. The current in vivo MEMRI approach may help evaluate, at high resolutions, the mechanisms guiding the establishment of topographically ordered connections in the central nervous system [4,8,92,103,109,134], the progressive changes in functional topology in diseases involving partial visual field loss, such as glaucoma, age-related macular degeneration, ischemic stroke and traumatic brain injury [28,115,[135][136][137][138][139][140] and the effect of interventions on neuronal rewiring upon early retinal and SC lesions [6,[105][106][107][108]141], all of which could eventually lead to new diagnostic techniques and therapies for improving visual impairments.…”