Induction of BDNF Expression in Layer II/III and Layer V Neurons of the Motor Cortex Is Essential for Motor Learning

Andreska, Thomas; Rauskolb, Stefanie; Schukraft, Nina; Lüningschrör, Patrick; Sasi, Manju; Signoret-Genest, Jérémy; Behringer, Marcus; Blum, Robert; Sauer, Markus; Tovote, Philip; Sendtner, Michael

doi:10.1523/jneurosci.0288-20.2020

Cited by 44 publications

(43 citation statements)

References 100 publications

(210 reference statements)

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“…We also found that a subset of BDNF-positive neurons in the motor cortex and the mPFC extends projections to the DLS. The motor cortex is known for innervating the DLS (Yin and Knowlton, 2006) and Andreska et al recently reported that BDNF in this corticostriatal circuit is essential for motor learning (Andreska et al, 2020). We show herein that OFC BDNF neurons project to the dorsal striatum.…”

Section: Characterization Of Corticostriatal Bdnf Neuronssupporting

confidence: 58%

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Identification of novel BDNF-specific corticostriatal circuitries

Ehinger

Soneja

Phamluong

et al. 2021

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BDNF is released from axon terminals originating in the cerebral cortex onto striatal neurons. Here, we characterized BDNF in the corticostriatal circuitry. First, we utilized Bdnf-Cre and Ribotag transgenic mouse lines to label BDNF-positive cells in the cortex, and detected BDNF expression in the motor cortex, medial prefrontal cortex (mPFC) and the orbitofrontal cortex (OFC). Next, we used a retrograde viral tracing strategy, in combination with Bdnf-Cre knockin mice, to map the cortical outputs of BDNF neurons in the dorsal striatum. We found that the BDNF-positive prefrontal regions differentially project to the dorsal striatum. Specifically, BDNF-expressing neurons located in the mPFC project to both dorsolateral striatum (DLS) and dorsomedial striatum (DMS), and those located in the motor cortex project to the DLS. Surprisingly however, the BDNF-expressing OFC neurons differentially target the dorsal striatum depending on their mediolateral location. Specifically, the DMS is mainly innervated by the medial part of the OFC (mOFC) whereas, the DLS receives projections specifically from the ventrolateral region of the OFC (vlOFC). Next, using an anterograde viral tracing strategy, we confirmed the presence of a BDNF-specific vlOFC-DLS circuit. Finally, we show that overexpression of BDNF in the vlOFC activates TrkB signaling specifically in the DLS but not in the DMS demonstrating the functionality of this circuit. Our study uncovers a previously unknown neural circuit composed of BDNF-positive vlOFC neurons projecting to the DLS. These findings could have important implications for the role of BDNF signaling in the OFC as well as in other corticostriatal circuitries.

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Section: Characterization Of Corticostriatal Bdnf Neuronssupporting

confidence: 58%

“…In the OFC, BDNF is critical for goal-directed decision making and in selecting actions based on their consequences (Gourley et al, 2013). In the motor cortex, BDNF contributes to motor learning (Andreska et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Identification of novel BDNF-specific corticostriatal circuitries

Ehinger

Soneja

Phamluong

et al. 2021

Preprint

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“…There have been several previous attempts to quantify neurophysiological markers of motor learning and performance (Baetu et al, 2015;Andreska et al, 2020;Herszage et al, 2020). Such attempts have included resting-state electroencephalography (EEG) activity, which has been shown to pre-dict visuomotor performance with the rotary pursuit task (Wu et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Resting-state aperiodic neural dynamics predict individual differences in visuomotor performance and learning

Immink

Cross

Chatburn

et al. 2021

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An emerging body of work has demonstrated that resting-state non-oscillatory, or aperiodic, 1/f neural activity is a functional and behaviorally relevant marker of cognitive function capacity. In the motor domain, previous work has only applied 1/f analyses to description of action coordination and performance. The value of aperiodic resting-state neural dynamics as a marker of individual visuomotor performance capacity remains unknown. Accordingly, the aim of this work was to investigate if individual 1/f intercept and slope parameters of aperiodic resting-state neural activity predict reaction time and perceptual sensitivity in an immersive virtual reality marksmanship task. The marksmanship task required speeded selection of target stimuli and avoidance of non-target stimuli selection. Motor and perceptual demands were incrementally increased across task blocks and participants performed the task across three training sessions spanning one week. When motor demands were high, steeper individual 1/f slope predicted shorter reaction time. This relationship did not change with practice. Increased 1/f intercept and a steeper 1/f slope were associated with higher perceptual sensitivity, measured as d′. However, this association was only observed under the highest levels of perceptual demand and only in the initial exposure to these conditions. Individuals with a lower 1/f intercept and a shallower 1/f slope demonstrated the greatest gains in perceptual sensitivity from task practice. These findings demonstrate that individual differences in motor and perceptual performance can be accounted for with resting-state aperiodic neural dynamics. The 1/f aperiodic parameters are most informative in predicting visuomotor performance under complex and demanding task conditions. In addition to predicting capacity for high visuomotor performance with a novel task, 1/f aperiodic parameters might also be useful in predicting which individuals might derive the most improvements from practice.

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“…Interestingly, the Sox6 gene contains a synaptic activity-responsive element (SARE), a regulatory enhancer element originally discovered in the immediate early gene Arc ( Kawashima et al, 2009 ) that predicts transcriptional changes in response to neuronal activation ( Rodriguez-Tornos et al, 2013 ; Pulimood et al, 2017 ). Therefore, to test the hypothesis that Sox6 expression in cortical Pvalb + cells can be modulated by increased network activity, we moved to the M1, a cortical region engaged during motor learning ( Kleim et al, 1996 , 1998 ; Beloozerova et al, 2003 ; Costa et al, 2004 ; Hosp et al, 2013 ; Cao et al, 2015 ; Andreska et al, 2020 ). We used the accelerating rotarod task as a means of enforcing locomotor activity and thus triggering increased neuronal firing in M1 ( Costa et al, 2004 ), which augments expression of activity-regulated genes in both pyramidal neurons ( Cao et al, 2015 ; Hirata et al, 2016 ) and in Pvalb + cells ( Arango-Lievano et al, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

Postnatal Sox6 Regulates Synaptic Function of Cortical Parvalbumin-Expressing Neurons

et al. 2021

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Cortical parvalbumin (Pvalb)-expressing neurons provide robust inhibition to neighboring pyramidal neurons, crucial for the proper functioning of cortical networks. This class of inhibitory neurons undergoes extensive synaptic formation and maturation during the first weeks after birth and continue to dynamically maintain their synaptic output throughout adulthood. While several transcription factors, such as Nkx2-1, Lhx6, and Sox6, are known to be necessary for the differentiation of progenitors into Pvalb + neurons, which transcriptional programs underlie the postnatal maturation and maintenance of Pvalb + neurons' innervation and synaptic function remains largely unknown. Because Sox6 is Significance statementCortical parvalbumin-expressing (Pvalb + ) inhibitory neurons provide robust inhibition to neighboring pyramidal neurons, crucial for the proper functioning of cortical networks. These inhibitory neurons undergo extensive synaptic formation and maturation during the first weeks after birth and continue to dynamically maintain their synaptic output throughout adulthood. However, it remains largely unknown which transcriptional programs underlie the postnatal maturation and maintenance of Pvalb + neurons. Here we show that the transcription factor Sox6 cell-autonomously regulates the synaptic maintenance and output of Pvalb + neurons until adulthood, leaving unaffected other maturational features of this neuronal population.

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Induction of BDNF Expression in Layer II/III and Layer V Neurons of the Motor Cortex Is Essential for Motor Learning

Cited by 44 publications

References 100 publications

Identification of novel BDNF-specific corticostriatal circuitries

Identification of novel BDNF-specific corticostriatal circuitries

Resting-state aperiodic neural dynamics predict individual differences in visuomotor performance and learning

Postnatal Sox6 Regulates Synaptic Function of Cortical Parvalbumin-Expressing Neurons

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