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Visual image motion-driven ocular motor behaviors such as the optokinetic reflex (OKR) provide sensory feedback for optimizing gaze stability during head/body motion. The performance of this visuo-motor reflex is subject to plastic alterations depending on requirements imposed by specific eco-physiological or developmental circumstances. While visuo-motor plasticity can be experimentally induced by various combinations of motion-related stimuli, the extent to which such evoked behavioral alterations contribute to the behavioral demands of an environment remains often obscure. Here, we used isolated preparations of Xenopus laevis tadpoles to assess the extent and ontogenetic dependency of visuo-motor plasticity during prolonged visual image motion. While a reliable attenuation of large OKR amplitudes can be induced already in young larvae, a robust response magnitude-dependent bidirectional plasticity is present only at older developmental stages. The possibility of older larvae to faithfully enhance small OKR amplitudes coincides with the developmental maturation of inferior olivary-Purkinje cell signal integration. This conclusion was supported by the loss of behavioral plasticity following transection of the climbing fiber pathway and by the immunohistochemical demonstration of a considerable volumetric extension of the Purkinje cell dendritic area between the two tested stages. The bidirectional behavioral alterations with different developmental onsets might functionally serve to standardize the motor output, comparable to the known differential adaptability of vestibulo-ocular reflexes in these animals. This homeostatic plasticity potentially equilibrates the working range of ocular motor behaviors during altered visuo-vestibular conditions or prolonged head/body motion to fine-tune resultant eye movements.
Fig. 1. Stimulation and recording of the optokinetic reflex in semi-intact preparations of Xenopus laevis tadpoles. a Schematic illustrating the experimental setting with a Ringer-filled circular recording chamber hosting the preparation; horizontal motion of vertical black and white stripes across the surrounding cylindrical screen serves as large-field visual motion stimulus and elicits eye movements (double arrows). b Representative example of horizontal positional oscillations of the eyes (lower trace) during prolonged (30 min) visual motion stimulation (upper traces), at the onset (left) and the end of the training period (right). c Single cycles of visual image motion profiles depicting the different combinations of stimulus velocities of either 4°/s (1, 4) or 8°/s (2, 3), presented in bidirectional alternation with a cycle duration of either 20 s (1, 2) or 10 s (3, 4)
Fig. 2. Ontogeny of OKR plasticity. a–f Differential effects of prolonged visual image motion in old (a–c) and young (d–f) larvae; individual eye motion cycles (gray traces) and population average (colored traces, n = 7 (old, a), n = 8 (young, d) at the onset (left) and the end (right) of prolonged visual motion stimulation with profile 1 (velocity: 4°/s, cycle duration: 20 s; see 1 in Fig. 1c); population-averaged response amplitudes across 30 min of training (b, e), measured on a per-cycle basis for stimulus paradigms 1–4, respectively; mean response of five cycles (c, f) obtained immediately (I) and at the end of the 30-min OKR entrainment (E) on a per-animal basis for stimulus paradigms 1–4 (performed on different, independent sets of naïve tadpoles, respectively; see Fig. 1c). g Amplitude changes plotted against immediate OKR amplitudes for old (blue) and young (orange) tadpoles; solid lines indicate linear regression fit to data; shaded areas indicate 95% confidence interval of the fit; horizontal dotted line indicates no amplitude change; dots above indicate OKR amplitude increase, dots below OKR amplitude decrease; blue (old tadpoles) and orange (young tadpoles) vertical dashed arrows indicate the theoretical initial amplitudes, above or below which a decrease or increase is expected. h Standard deviation (SD) of the averaged response amplitudes immediately (I) and at the end of the entrainment period (E) for old and young tadpoles and stimulus paradigms 1–4 (for color-code see b, e). i Violin plots of immediate (I) and entrained response amplitudes (E), in young and old tadpoles respectively, pooled across stimulation paradigms 1–4
Fig. 3. Anatomical and functional consequences of climbing fiber transection. a Schematic of a Xenopus tadpole brain depicting the direct (black) and indirect (blue) OKR pathways for eliciting a horizontal OKR during rightward motion stimulation of the right eye; the site of climbing fiber transection in the caudal hindbrain is indicated by the green dashed line. b–e Whole-mount confocal reconstructions of the hindbrain (Hb) of a stage 55 control tadpole (b–c) and after midline transection (d–e) at the level of the caudal hindbrain (green line in a, scheme in d) counterstained with DAPI (blue nuclei); unilateral cerebellar injections of Tetramethylrhodamine (TMR; black arrows), outlined the climbing fiber (CF) axonal pathway (green arrow heads in c, e) and parent inferior olivary cell bodies in the contralateral ventral hindbrain in controls (b) and lack thereof after the lesion (* in d), illustrated at higher magnification in c, e (green dashed rectangles); f Population-averaged response amplitudes across 30 min of training, measured on a per-cycle basis for stimulus paradigms 3 and 4, in controls (blue) and after CF transection (green). g Mean response of five cycles obtained immediately (I) and at the end of the 30-min OKR entrainment (E) on a per-animal basis for stimulus paradigms 3 and 4 (see Fig. 1c) in CF-transected animals. h Amplitude changes plotted against immediate OKR amplitudes for controls (blue) and CF-transected animals (green); solid lines indicate linear regression fit to data, and shaded area the 95% confidence interval of the fit; horizontal dotted line indicates no amplitude change; dots above the line indicate amplitude increase, dots below amplitude decrease. Blue (control tadpoles) and green (CF-transected tadpoles) vertical dashed arrows indicate the theoretical initial amplitudes, above or below which a decrease or increase is expected. Abd abducens nucleus, Cb cerebellum, D dorsal, IO inferior olive, L lateral, MN motoneurons, Ocu oculomotor nucleus, Pt pretectum, R rostral, VN vestibular nuclei. Scale bars in all panels represent 100 µm
Fig. 4. Ontogenetic plasticity of calbindin- and glutamate-decarboxylase (GAD67)-immunopositive cerebellar structures. a–f Parasagittal sections at two medio-lateral planes (see scheme on top in a) through the hindbrain (Hb) depicting calbindin- (green) and GAD67-labeled (red) and DAPI-counterstained (blue) morphological structures in young (a–c) and old tadpoles (d–f); medially (M in scheme on top in a) located sagittal sections depicting overviews (a, d) and higher magnifications (b, e) of calbindin- and GAD67-immunopositive structures in the hindbrain and cerebellum (Cb); laterally (L in scheme on top in a) located sagittal sections (c, f) depicting respective immunopositive elements in the lateral cerebellum of young (c) and old (f) tadpoles. g, h Coronal sections at the level of the cerebellum of young (g) and old (h) tadpoles, outlining the region used to measure the location of Purkinje cell (PC) somata (white) and the extension of the dendritic tree (gray). i Quantification of the volumes of Purkinje cell somata (left), dendritic tree (middle) and ratio of dendritic tree/Purkinje cell somatic volumes (right) in young and old tadpoles. OT optic tectum, R rostral, V ventral, IVth fourth ventricle. Scale bars in all panels represent 100 µm
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