Competitive and cooperative interactions between medial temporal and striatal learning systems

Freedberg, Michael; Toader, Andrew C.; Wassermann, Eric M.; Voss, Joel L.

doi:10.1016/j.neuropsychologia.2019.107257

Cited by 34 publications

(29 citation statements)

References 183 publications

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“…Together with the observation of inhibitory-stimulation-induced increases in fronto-hippocampal connectivity over the course of learning, the present results indicate that inhibitory prefrontal cTBS promoted the progressive engagement of networks involved in early learning and control processes. It is worth noting that we did not observe any stimulation-induced changes in hippocampo-striatal functional connectivity, such as a decrease in competition between the two networks, as recently proposed by Freedberg et al (2020).…”

Section: Dlpfc Stimulation Influenced Connectivity In Fronto-hippocamsupporting

confidence: 80%

“…Importantly, functional connectivity between these networks reveals a competitive interaction pattern during this initial learning stage (Albouy, King, et al, 2013;. Crucial to the present study, this interaction between hippocampal and striatal systems is thought to be orchestrated by the dorsolateral prefrontal cortex (DLPFC) (Albouy, King, et al, 2013;Albouy et al, 2012;Freedberg, Toader, Wassermann, & Voss, 2020).…”

Section: Introductionmentioning

confidence: 67%

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Hippocampal and striatal responses during motor learning are modulated by prefrontal cortex stimulation

Gann

King

Dolfen

et al. 2020

Preprint

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While it is widely accepted that motor sequence learning (MSL) is supported by a prefrontal-mediated interaction between hippocampal and striatal networks, it remains unknown whether the functional responses of these networks can be modulated in humans with targeted experimental interventions. The present proofof-concept study employed a comprehensive multimodal neuroimaging approach, including functional magnetic resonance (MR) imaging and MR spectroscopy, to investigate whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex can modulate responses in the hippocampus and striatum during motor learning. Our results indicate that stimulation influenced task-related connectivity patterns within hippocampo-frontal and striatal networks. Stimulation also altered the relationship between the levels of gamma-aminobutyric acid (GABA) in the stimulated prefrontal cortex and learning-related changes in both activity and connectivity in fronto-striato-hippocampal networks. This study provides the first experimental evidence that brain stimulation can alter motor learning-related functional responses in the striatum and hippocampus.

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Section: Dlpfc Stimulation Influenced Connectivity In Fronto-hippocamsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 67%

Hippocampal and striatal responses during motor learning are modulated by prefrontal cortex stimulation

Gann

King

Dolfen

et al. 2020

Preprint

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“…These findings are in line with computational models proposing that the hippocampus rapidly forms associations between stimuli, the basal ganglia gradually learns associations over time, and prefrontal cortex mediates interaction between these regions (Atallah et al, 2004;McClelland et al, 1995). Based on these models, one might predict a cooperative (positive) or competitive (negative) relationship between hippocampus and basal ganglia activity (Freedberg et al, 2020), particularly during early IAL when they are both engaged in learning associations. Most studies that have correlated IAL-related activity in these regions collapsed across all learning stages (Dennis and Cabeza, 2011;Poldrack et al, 2001;Rieckmann et al, 2010;Seger and Cincotta, 2005;Stillman et al, 2016b), but two studies found cooperative relationships during the peak of learning that decoupled over the course of learning Stark, 2015, 2011) and another showed that these hippocampus-basal ganglia interactions were mediated by activity in the prefrontal cortex across learning stages (Poldrack and Rodriguez, 2004).…”

supporting

confidence: 83%

“…These findings indicate more coordinated IALrelated activity between the hippocampus and basal ganglia in younger adults that starts early in learning and extends across multiple basal ganglia nuclei. This may reflect younger adults preferentially recruiting these neural systems to work cooperatively early in the task to learn associations, compared to later in learning when the associations may be consolidated into memories (Freedberg et al, 2020;Stark, 2015, 2011). In contrast, aging of these individual brain regions may lead to functional reorganization of the interactive networks needed to learn associations, affecting the regional specificity and time course of inter-region communication in older adults (Guye et al, 2008), and ultimately their IAL performance.…”

Section: Discussionmentioning

confidence: 99%

Age group differences in learning-related activity reflect task stage, not learning stage

Merenstein¹,

Petok²,

Bennett³

2020

Preprint

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Healthy aging is accompanied by declines in our ability to learn associations between events without awareness, termed implicit associative learning (IAL). Previous functional magnetic resonance imaging (fMRI) studies have attributed these learning deficits in older adults to differential engagement of the hippocampus, basal ganglia, and prefrontal cortex relative to younger adults. But it remains unclear whether there are also age group differences in how these brain regions coordinate learning of associations over time. Here, we acquired fMRI data while 28 younger (20.8 ± 2.3 years) and 22 older (73.6 ± 6.8 years) healthy adults completed the Triplets Learning Task, in which the location of two cues predicted the location of a target with high (HF) or low (LF) frequency. Results revealed significant age group differences in learning as smaller difference in reaction time to HF versus LF triplets in older relative to younger adults, and in the recruitment of hippocampal and prefrontal regions during early learning. Moreover, learning-related activity was significantly related among hippocampal, basal ganglia, and prefrontal regions for both age groups, although younger adults exhibited stronger hippocampal-basal ganglia interactions during early learning whereas older adults showed stronger prefrontal-hippocampal interactions during late learning. Thus, age-related declines in the ability to learn implicit associations may result from both differential engagement of and coordination between these brain regions, which are traditionally thought to comprise separate learning systems.

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“…Hence, event file coding might depend on the strength of associations between stimuli (object files) and responses (action files), as the partial repetition costs are particularly high when (strong) pre-established bindings persist. Since the GABAergic system seems to play an important role for response selection, it is conceivable that the planned correlation analysis reveals a different pattern as the task progresses: The striatum and especially the striatal GABAergic system have repeatedly been suggested to play a role in acquiring S-R associations (Freedberg, Toader, Wassermann, & Voss, 2020;Graybiel & Grafton, 2015;Kreitzer & Malenka, 2008;Miyachi, Hikosaka, Miyashita, Kárádi, & Rand, 1997;Perrin & Venance, 2019;Schumacher, de Vasconcelos, Lecourtier, Moser, & Cassel, 2011). Therefore, the functional role of striatal GABA might be different for event file coding in early and late phases of the task.…”

mentioning

confidence: 99%

On the functional role of striatal and anterior cingulateGABA+ in stimulus‐response binding

Takács

Stock

Kuntke

et al. 2021

Human Brain Mapping

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Successful response selection relies on constantly updating stimulus–response associations. The Theory of Event Coding (TEC) proposes that perception and action are conjointly coded in event files, for which fronto‐striatal networks seem to play an important role. However, the exact neurobiochemical mechanism behind event file coding has remained unknown. We investigated the functional relevance of the striatal and anterior cingulate (ACC) GABAergic system using magnetic resonance spectroscopy (MRS). Specifically, the striatal and ACC concentrations of GABA+ referenced against N‐acetylaspartate (NAA) were assessed in 35 young healthy males, who subsequently performed a standard event file task. As predicted by the TEC, the participants' responses were modulated by pre‐established stimulus response bindings in event files. GABA+/NAA concentrations in the striatum and ACC were not correlated with the overall event binding effect. However, higher GABA+/NAA concentrations in the ACC were correlated with stronger event file binding processes in the early phase of the task. This association disappeared by the end of the task. Taken together, our findings show that striatal GABA+ levels does not seem to modulate event file binding, while ACC GABA+ seem to improve event file binding, but only as long as the participants have not yet gathered sufficient task experience. To the best of our knowledge, this is the first study providing direct evidence for the role of striatal and ACC GABA+ in stimulus–response bindings and thus insights into the brain structure‐specific neurobiological aspects of the TEC.

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Competitive and cooperative interactions between medial temporal and striatal learning systems

Cited by 34 publications

References 183 publications

Hippocampal and striatal responses during motor learning are modulated by prefrontal cortex stimulation

Hippocampal and striatal responses during motor learning are modulated by prefrontal cortex stimulation

Age group differences in learning-related activity reflect task stage, not learning stage

On the functional role of striatal and anterior cingulateGABA+ in stimulus‐response binding

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