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Humanized Foxp2 accelerates learning by enhancing transitions from declarative to procedural performance.

ABSTRACT: The acquisition of language and speech is uniquely human, but how genetic changes might have adapted the nervous system to this capacity is not well understood. Two human-specific amino acid substitutions in the transcription factor forkhead box P2 (FOXP2) are outstanding mechanistic candidates, as they could have been positively selected during human evolution and as FOXP2 is the sole gene to date firmly linked to speech and language development. When these two substitutions are introduced into the endogenous Foxp2 gene of mice (Foxp2(hum)), cortico-basal ganglia circuits are specifically affected. Here we demonstrate marked effects of this humanization of Foxp2 on learning and striatal neuroplasticity. Foxp2(hum/hum) mice learn stimulus-response associations faster than their WT littermates in situations in which declarative (i.e., place-based) and procedural (i.e., response-based) forms of learning could compete during transitions toward proceduralization of action sequences. Striatal districts known to be differently related to these two modes of learning are affected differently in the Foxp2(hum/hum) mice, as judged by measures of dopamine levels, gene expression patterns, and synaptic plasticity, including an NMDA receptor-dependent form of long-term depression. These findings raise the possibility that the humanized Foxp2 phenotype reflects a different tuning of corticostriatal systems involved in declarative and procedural learning, a capacity potentially contributing to adapting the human brain for speech and language acquisition.

SUBMITTER: Schreiweis C

PROVIDER: S-EPMC4191787 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Humanized Foxp2 Accelerates Making Transitions From Declarative to Procedural Learning

Project description:Purpose: Foxp2 is the first and for now the only gene connected to speech and language in humans. Two aminoacid substitutions took place in this protein during recent human evolution, after our split from the last common ancestor with chimpanzees, and are most likely to have undergone positive selection in human lineage (Enard et al., 2002). Methods: Transgenic mice in which the wild-type (murine) version of Foxp2 was replaced with the one bearing two human-specific amino acid substitutions (i.e. "humanized" Foxp2) - Foxp2hum/hum, have been compared to their wild-type (WT) counterparts in terms of behavior, electrophysiology and striatal gene expression. The latter was analyzed through RNA-sequencing performed on pooled indexed libraries on three flow cells on Illumina GAIIx. The reads were mapped to mouse genome (mm9) by TopHat 1.4.1 and were counted using Bedtools. mRNA profiles were obtained with more than 20 million reads for every sample. Differential gene expression was analyzed with DESeq using multifactor model (Anders and Huber, 2010). Results: Wild-type and Foxp2hum/hum mice did not show any significant differences in expression at individual gene level, neither in dorsomedial nor in dorsolateral striatum. However, when genes were grouped into functional categories and analyzed accordingly, this revealed a significant downregulation of functional categories related to synaptic signalling and plasticity in dorsomedial striatum of Foxp2hum/hum mice. RNA-sequencing was performed on dorsomedial and dorsolateral striatum of wild-type and Foxp2hum/hum mice, on three flow cells Illumina GAIIx. The libraries from each sample were indexed and pooled together.

2014-09-24 | E-GEOD-60659 | biostudies-arrayexpress

Humanized Foxp2 Accelerates Making Transitions From Declarative to Procedural Learning

2014-09-24 | GSE60659 | GEO

Does Acute Stress Impact Declarative and Procedural Learning?

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Enhanced procedural learning of speech sound categories in a genetic variant of FOXP2.

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Project description:A recent study has established that thinkers reliably engage in epistemic appraisals of concepts of natural categories. Here, five studies are reported which investigated the effects of different manipulations of category learning context on appraisal of the concepts learnt. It was predicted that dimensions of concept appraisal could be affected by manipulating either procedural factors (spacing of learning, perceptual fluency) or declarative factors (causal knowledge about categories). While known effects of these manipulations on metacognitive judgements such as category learning judgements and confidence at test were replicated, procedural factors had no reliable effects on the dimensions of concept appraisal. Effects of declarative manipulations on some forms of concept appraisal were observed.

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Project description:According to the Declarative/Procedural Model, the lexicon depends on declarative memory while grammar relies on procedural memory. Furthermore, procedural memory underlies the sequential processing of language. Thus, this system is important for predicting the next item in a sentence. Verb processing represents a good candidate to test this assumption. Semantic representations of verbs include information about the protagonists in the situations they refer to. This semantic knowledge is acquired implicitly and used during verb processing, such that the processing of a verb preactivates its typical patients (e.g., the window for break). Thus, determining how the patient typicality effect appears during children's cognitive development could provide evidence about the memory system that is dedicated to this effect. Two studies are presented in which French children aged 6-10 and adults made grammaticality judgments on 80 auditorily presented sentences. In Experiment 1, the verb was followed by a typical patient or by a less typical patient. In Experiment 2, grammatical sentences were constructed such that the verb was followed either by a typical patient or by a noun that could not be a patient of that verb. The typicality effect occurs in younger children and is interpreted in terms of developmental invariance. We suggest that this effect may depend on procedural memory, in line with studies that showed that meaning is necessary to allow procedural memory to learn the sequence of words in a sentence.

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Project description:Declarative memory and procedural memory are known to be two fundamentally different kinds of memory that are dissociable in their psychological characteristics and measurement (explicit vs. implicit) and in the neural systems that subserve each kind of memory. Declarative memory abilities are known to improve from childhood through young adulthood, but the developmental maturation of procedural memory is largely unknown. We compared 10-year-old children and young adults on measures of declarative memory and working memory capacity and on four measures of procedural memory that have been strongly dissociated from declarative memory (mirror tracing, rotary pursuit, probabilistic classification, and artificial grammar). Children had lesser declarative memory ability and lesser working memory capacity than adults, but children exhibited learning equivalent to adults on all four measures of procedural memory. Therefore, declarative memory and procedural memory are developmentally dissociable, with procedural memory being adult-like by age 10years and declarative memory continuing to mature into young adulthood.

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