Rapid Plasticity of Visual Responses in the Adult Lateral Geniculate Nucleus

Center for Neuroscience, University of California, Davis, Davis, CA 95618, USA.
Neuron (Impact Factor: 15.05). 09/2011; 71(5):812-9. DOI: 10.1016/j.neuron.2011.06.025
Source: PubMed


Compared to the developing visual system, where neuronal plasticity has been well characterized at multiple levels, little is known about plasticity in the adult, particularly within subcortical structures. We made intraocular injections of 2-amino-4-phosphonobutyric acid (APB) in adult cats to block visual responses in On-center retinal ganglion cells and examined the consequences on visual responses in the lateral geniculate nucleus (LGN) of the thalamus. In contrast to current views of retinogeniculate organization, which hold that On-center LGN neurons should become silent with APB, we find that ∼50% of On-center neurons rapidly develop Off-center responses. The time course of these emergent responses and the actions of APB in the retina indicate the plasticity occurs within the LGN. These results suggest there is greater divergence of retinogeniculate connections than previously recognized and that functionally silent, nonspecific retinal inputs can serve as a substrate for rapid plasticity in the adult.

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Available from: W. Martin Usrey
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    • "In addition, the LGB is known to be connected to the parietal and temporal lobes for unconscious vision (blindsight) [15]. Therefore, the LGB has been suggested to have an important role in brain plasticity of the visual system following brain injury [15] [19] [25]. However, little is known about the neural connectivity of the LGB in the human brain. "
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    ABSTRACT: A few studies have reported on the neural connectivity of some neural structures of the visual system in the human brain. However, little is known about the neural connectivity of the lateral geniculate body (LGB). In the current study, using diffusion tensor tractography (DTT), we attempted to investigate the neural connectivity of the LGB in normal subjects. A total of 52 healthy subjects were recruited for this study. A seed region of interest was placed on the LGB using the FMRIB Software Library which is a probabilistic tractography method based on a multi-fiber model. Connectivity was defined as the incidence of connection between the LGB and target brain areas at the threshold of 5, 25, and 50 streamlines. In addition, connectivity represented the percentage of connection in all hemispheres of 52 subjects. We found the following characteristics of connectivity of the LGB at the threshold of 5 streamline: (1) high connectivity to the corpus callosum (91.3%) and the contralateral temporal cortex (56.7%) via the corpus callosum, (2) high connectivity to the ipsilateral cerebral cortex: the temporal lobe (100%), primary visual cortex (95.2%), and visual association cortex (77.9%). The LGB appeared to have high connectivity to the corpus callosum and both temporal cortexes as well as the ipsilateral occipital cortex. We believe that the results of this study would be helpful in investigation of the neural network associated with the visual system and brain plasticity of the visual system after brain injury.
    Full-text · Article · Jun 2014 · Neuroscience Letters
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    • "The other explanation is that a single LGN neuron receives convergent inputs from multiple RGCs sharing in-line RF positions that elongate the RF of the LGN neuron (Tavazoie and Reid, 2000). Several studies have shown the possibility of convergent inputs in retinogeniculate connections (Usrey et al., 1999; Moore et al., 2011), which are important for creating a diversity of RF structures in different LGN neurons (Alonso et al., 2006). However, it is still unclear how convergent projections in retinogeniculate connections contribute to the spatial and temporal RF structure of LGN neurons. "
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    ABSTRACT: The spatial structure of the receptive field (RF) of cat lateral geniculate nucleus (LGN) neurons is significantly elliptical, which may provide a basis for the orientation tuning of LGN neurons, especially at high spatial frequency stimuli. However, the input mechanisms generating this elliptical RF structure are poorly defined. We therefore compared the spatiotemporal RF structures of pairs of retinal ganglion cells (RGCs) and LGN neurons that form monosynaptic connections based on the cross-correlation analysis of their firing activities. We found that the spatial RF structure of both RGCs and LGN neurons were comparably elliptical and oriented in a direction toward the area centralis. Additionally, the spatial RF structures of pairs with the same response sign were often overlapped and similarly oriented. We also found there was a small population of pairs with RF structures that had the opposite response sign and were spatially displaced and independently oriented. Finally, the temporal RF structure of an RGC was tightly correlated with that of its target LGN neuron, though the response duration of the LGN neuron was significantly longer. Our results suggest that the elliptical RF structure of an LGN neuron is mainly inherited from the primary projecting RGC and is affected by convergent inputs from multiple RGCs. We discuss how the convergent inputs may enhance the stimulus feature sensitivity of LGN neurons.
    Full-text · Article · Dec 2013 · Frontiers in Systems Neuroscience
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    • "Moreover, the NOT-DTN may receive an additional as yet undetected input from OFF direction selective ganglion cells and from ON/OFF ganglion cells as recently described for the mouse [21]. Alternatively, local mechanisms in the NOT-DTN enhancing normally silent neuronal connections in case of a decreased ON input may cause our increased OFF response [58]. "
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    ABSTRACT: In the present study we investigated in vivo the effects of pharmacological manipulation of retinal processing on the response properties of direction selective retinal slip cells in the nucleus of the optic tract and dorsal terminal nucleus (NOT-DTN), the key visuomotor interface in the pathway underlying the optokinetic reflex. Employing a moving visual stimulus consisting of either a large dark or light edge we could differentiate direction selective ON and OFF responses in retinal slip cells. To disclose the origin of the retinal slip cells' unexpected OFF response we selectively blocked the retinal ON channels and inactivated the visual cortex by cooling. Cortical cooling had no effect on the direction selectivity of the ON or the OFF response in NOT-DTN retinal slip cells. Blockade of the retinal ON channel with APB led to a loss of the ON and, to a lesser degree, of the OFF response and a reduction in direction selectivity. Subsequent blocking of GABA receptors in the retina with picrotoxin unmasked a vigorous albeit direction unselective OFF response in the NOT-DTN. Disturbing the retinal chloride homeostasis by intraocular injections of bumetanide or furosemide led to a loss of direction selectivity in both the NOT-DTN's ON and the OFF response due to a reduced response in the neuron's preferred direction under bumetanide as well as under furosemide and a slightly increased response in the null direction under bumetanide. Our results indicate that the direction specificity of retinal slip cells in the NOT-DTN of the rat strongly depends on direction selective retinal input which depends on intraretinal chloride homeostasis. On top of the well established input from ON center direction selective ganglion cells we could demonstrate an equally effective input from the retinal OFF system to the NOT-DTN.
    Full-text · Article · Sep 2012 · PLoS ONE
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