Somatosensory map expansion and altered processing of tactile inputs in a mouse model of fragile X syndrome

Juczewski, Konrad; Richthofen, Helen J. von; Bagni, Claudia; Celikel, Tansu; Fisone, Gilberto; Krieger, Patrik

doi:10.1016/j.nbd.2016.09.007

Cited by 50 publications

(65 citation statements)

References 298 publications

(289 reference statements)

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“…Interestingly, increased excitability along the intracortical projections facilitates the integration of sensory information across whisk cycles such that Sert −/− rats required fewer whisker touch and showed faster response times compared Sert +/+ rats. These results are in agreement with recent observations in a mouse of Fragile X syndrome (Juczewski et al 2016) where hyperexcitability of the primary somatosensory neurons have been well characterized (Zhang et al 2014; Juczewski et al 2016). Collectively, the findings point to an inverse correlation between somatosensory cortical excitability and the duration of tactile sampling required for successful object localization by whisker contacts.…”

Section: Discussionsupporting

confidence: 93%

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Reduced Inhibition within Layer IV of Sert Knockout Rat Barrel Cortex is Associated with Faster Sensory Integration

et al. 2017

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Neural activity is essential for the maturation of sensory systems. In the rodent primary somatosensory cortex (S1), high extracellular serotonin (5-HT) levels during development impair neural transmission between the thalamus and cortical input layer IV (LIV). Rodent models of impaired 5-HT transporter (SERT) function show disruption in their topological organization of S1 and in the expression of activity-regulated genes essential for inhibitory cortical network formation. It remains unclear how such alterations affect the sensory information processing within cortical LIV. Using serotonin transporter knockout (Sert−/−) rats, we demonstrate that high extracellular serotonin levels are associated with impaired feedforward inhibition (FFI), fewer perisomatic inhibitory synapses, a depolarized GABA reversal potential and reduced expression of KCC2 transporters in juvenile animals. At the neural population level, reduced FFI increases the excitatory drive originating from LIV, facilitating evoked representations in the supragranular layers II/III. The behavioral consequence of these changes in network excitability is faster integration of the sensory information during whisker-based tactile navigation, as Sert−/− rats require fewer whisker contacts with tactile targets and perform object localization with faster reaction times. These results highlight the association of serotonergic homeostasis with formation and excitability of sensory cortical networks, and consequently with sensory perception.

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Section: Discussionsupporting

confidence: 93%

“…7 A ). Tactile exploration of the target platform was observed using high-speed infrared imaging (Voigts et al 2008; Pang et al 2011; Juczewski et al 2016) and tactile evidence (i.e., duration of whisker contact; Fig. 7 B ) before successful object localization was quantified using video recordings (see Materials and Methods; Fig.…”

Section: Resultsmentioning

confidence: 99%

Reduced Inhibition within Layer IV of Sert Knockout Rat Barrel Cortex is Associated with Faster Sensory Integration

et al. 2017

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“…The whisker system, with its modular organization along the whiskerto-barrel pathway as well as the rich behavioral repertoire of whisker dependent tasks (e.g. (Filipkowski et al, 2000;Guic-Robles et al, 1992;Jabłońska and Skangiel-Kramska, 1995;Jacobs and Juliano, 1995); (Celikel and Sakmann, 2007;Clem et al, 2008;Cohen and Castro-Alamancos, 2010;Galvez et al, 2007;Grion et al, 2016;Guic et al, 2008;Juczewski et al, 2016;Krupa et al, 2001;Miceli et al, 2017;Miyashita and Feldman, 2013;O'Connor et al, 2010;Rosselet et al, 2011;Safaai et al, 2013;Topchiy et al, 2009;Troncoso et al, 2007;Voigts et al, 2015;Waiblinger et al, 2015)), will likely lead the way.…”

Section: ) From Synaptic Plasticity To Synaptic Disordersmentioning

confidence: 99%

Cellular diversity of the somatosensory cortical map plasticity

Kole

Scheenen

Tiesinga

et al. 2018

Neuroscience & Biobehavioral Reviews

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Sensory maps are representations of the sensory epithelia in the brain. Despite the intuitive explanatory power behind sensory maps as being neuronal precursors to sensory perception, and sensory cortical plasticity as a neural correlate of perceptual learning, molecular mechanisms that regulate map plasticity are not well understood. Here we perform a meta-analysis of transcriptional and translational changes during altered whisker use to nominate the major molecular correlates of experience-dependent map plasticity in the barrel cortex. We argue that brain plasticity is a systems level response, involving all cell classes, from neuron and glia to non-neuronal cells including endothelia. Using molecular pathway analysis, we further propose a gene regulatory network that could couple activity dependent changes in neurons to adaptive changes in neurovasculature, and finally we show that transcriptional regulations observed in major brain disorders target genes that are modulated by altered sensory experience. Thus, understanding the molecular mechanisms of experience-dependent plasticity of sensory maps might help to unravel the cellular events that shape brain plasticity in health and disease. peer-reviewed)

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“…Finally, if the experimental design requires targeted alteration of molecular/cellular function, upon, e.g., sensory deprivation (Celikel et al, 2004;Foeller, Celikel, & Feldman, 2005), induction of synaptic plasticity in identified pathways (Allen et al, 2003;Clem, Celikel, & Barth, 2008), systematic modulation of cellular excitability (Huang et al, 2016;Juczewski et al, 2016;Miceli et al, 2017), circuit alterations (Corsini et al, 2009;Freudenberg et al, 2013aFreudenberg et al, , 2013bFreudenberg et al, , 2016Seib et al, 2013), or behavioral training (Celikel & Sakmann, 2007;Seib et al, 2013;Voigts, Herman, & Celikel, 2015), it would be advisable to design the experiments to ensure availability of within-animal and within-slice (wherever applicable) controls to minimize the genomic variability across independent samples and the experimental groups.…”

Section: Of 21mentioning

confidence: 99%

Neocortical Microdissection at Columnar and Laminar Resolution for Molecular Interrogation

Kole

Celikel

2018

CP Neuroscience

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The heterogeneous organization of the mammalian neocortex poses a challenge for elucidating the molecular mechanisms underlying its physiological processes. Although high‐throughput molecular methods are increasingly deployed in neuroscience, their anatomical specificity is often lacking. In this unit, we introduce a targeted microdissection technique that enables extraction of high‐quality RNA and proteins at high anatomical resolution from acutely prepared brain slices. We exemplify its utility by isolating single cortical columns and laminae from the mouse primary somatosensory (barrel) cortex. Tissues can be isolated from living slices in minutes, and the extracted RNA and protein are of sufficient quantity and quality to be used for RNA sequencing and mass spectrometry. This technique will help to increase the anatomical specificity of molecular studies of the neocortex, and the brain in general, as it is applicable to any brain structure that can be identified using optical landmarks in living slices. © 2018 by John Wiley & Sons, Inc.

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Somatosensory map expansion and altered processing of tactile inputs in a mouse model of fragile X syndrome

Cited by 50 publications

References 298 publications

Reduced Inhibition within Layer IV of Sert Knockout Rat Barrel Cortex is Associated with Faster Sensory Integration

Reduced Inhibition within Layer IV of Sert Knockout Rat Barrel Cortex is Associated with Faster Sensory Integration

Cellular diversity of the somatosensory cortical map plasticity

Neocortical Microdissection at Columnar and Laminar Resolution for Molecular Interrogation

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