Frontal Networks for Learning and Executing Arbitrary Stimulus-Response Associations

Department of Psychology, University of California, Berkeley, Berkeley, California, United States
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.75). 04/2005; 25(10):2723-32. DOI: 10.1523/JNEUROSCI.3697-04.2005
Source: PubMed

ABSTRACT Flexible rule learning, a behavior with obvious adaptive value, is known to depend on an intact prefrontal cortex (PFC). One simple, yet powerful, form of such learning consists of forming arbitrary stimulus-response (S-R) associations. A variety of evidence from monkey and human studies suggests that the PFC plays an important role in both forming new S-R associations and in using learned rules to select the contextually appropriate response to a particular stimulus cue. Although monkey lesion studies more strongly implicate the ventrolateral PFC (vlPFC) in S-R learning, clinical data and neurophysiology studies have implicated both the vlPFC and the dorsolateral region (dlPFC) in associative rule learning. Previous human imaging studies of S-R learning tasks, however, have not demonstrated involvement of the dlPFC. This may be because of the design of previous imaging studies, which used few stimuli and used explicitly stated one-to-one S-R mapping rules that were usually practiced before scanning. Humans learn these rules very quickly, limiting the ability of imaging techniques to capture activity related to rule acquisition. To address these issues, we performed functional magnetic resonance imaging while subjects learned by trial and error to associate sets of abstract visual stimuli with arbitrary manual responses. Successful learning of this task required discernment of a categorical type of S-R rule in a block design expected to yield sustained rule representation. Our results show that distinct components of the dorsolateral, ventrolateral, and anterior PFC, lateral premotor cortex, supplementary motor area, and the striatum are involved in learning versus executing categorical S-R rules.

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Available from: Charlotte A Boettiger, Aug 08, 2015
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    • "Previous research suggests that functions discussed above might also apply to the right caudate nucleus. Specifically, it might have been involved in representing S–R rules (Toni and Passingham 1999; Passingham et al. 2000; Toni et al. 2001; Boettiger and D'Esposito 2005) and/or selecting (Schumacher et al. 2003; Gerardin et al. 2004; Wager et al. 2005; van Eimeren et al. 2006; Amiez et al. 2012) and reprogramming (Mars et al. 2007) the relevant response appropriate to the target. These possible functions would be relied on less during CON compared with INC trials. "
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    ABSTRACT: Unconscious visuomotor priming defined as the advantage in reaction time (RT) or accuracy for target shapes mapped to the same (congruent condition) when compared with a different (incongruent condition) motor response as a preceding subliminally presented prime shape has been shown to modulate activity within a visuomotor network comprised of parietal and frontal motor areas in previous functional magnetic resonance imaging (fMRI) studies. The present fMRI study investigated whether, in addition to changes in brain activity, unconscious visuomotor priming results in a modulation of functional connectivity profiles. Activity associated with congruent compared with incongruent trials was lower in the bilateral inferior and medial superior frontal gyri, in the inferior parietal lobules, and in the right caudate nucleus and adjacent portions of the thalamus. Functional connectivity increased under congruent relative to incongruent conditions between ventral visual stream areas (e.g., calcarine, fusiform, and lingual gyri), the precentral gyrus, the supplementary motor area, posterior parietal areas, the inferior frontal gyrus, and the caudate nucleus. Our findings suggest that an increase in coupling between visuomotor regions, reflecting higher efficiency of processing, is an important neural mechanism underlying unconscious visuomotor priming, in addition to changes in the magnitude of activation. © The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail:
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    • "In our experiment, we demonstrated that (i) DS does not mediate early feedback-based stimulus–response learning but is implicated in performing response decisions, and (ii) VS underlies stimulus–response association learning. Our findings challenge the claim that DS mediates stimulus–response learning via feedback (Balleine et al., 2009; Boettiger and D'Esposito, 2005; Brovelli et al., 2011; Brown and Stern, 2013; Foerde et al., 2013; Garrison et al., 2013; Hart et al., 2014), and recast it as a brain region mediating decision making, integrating with a growing literature supporting this view (Atallah et al., 2007; Grahn et al., 2008; Jessup and O'Doherty, 2011; MacDonald et al., 2014; McDonald and Hong, 2004; Postle and D'Esposito, 1999; Smittenaar et al., 2012). "
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    • "Electrophysiological and neuropsychological studies in nonhuman primates have identified regions that support both the acquisition and the retention of conditional visuomotor associations, including the medial temporal lobe (MTL) (Murray and Wise 1996; Wise and Murray 1999, 2000; Brasted et al. 2003; Wirth et al. 2003; Yanike et al. 2009), premotor cortex (Halsband and Passingham 1985; Mitz et al. 1991; Brasted and Wise 2004; Buch et al. 2006), prefrontal cortex (Murray et al. 2000; Wang et al. 2000; Bussey et al. 2001; Pasupathy and Miller 2005; Histed et al. 2009), and the striatum (Canavan et al. 1989; Hadj-Bouziane and Boussaoud 2003; Hadj- Bouziane et al. 2003, 2006; Brasted and Wise 2004; Nixon et al. 2004; Pasupathy and Miller 2005; Buch et al. 2006; Williams and Eskandar 2006; Histed et al. 2009). fMRI studies utilizing arbitrary associative learning tasks have reported changes in cerebral blood flow across a similar network of regions (Toni et al. 2001; Eliassen et al. 2003; Boettiger and D'Esposito 2005; Law et al. 2005; Grol et al. 2006; Hanakawa et al. 2006; Haruno and Kawato 2006; Brovelli et al. 2008). Many of the regions identified in these studies were posited to support learning via different computational goals. "
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    ABSTRACT: A network of regions including the medial temporal lobe (MTL) and the striatum are integral to visuomotor associative learning. Here, we evaluated the contributions of the structures of the striatum and the MTL, as well as their interactions during an arbitrary associative learning task. We hypothesized that activity in the striatum would correlate with the rate of learning, while activity in the MTL would track how well associations were learned. Further, we expected functional correlations to show both facilitative as well as competitive relationships depending on the regions involved. Results showed that activity throughout the striatum was modulated by the rate of learning, while the sensorimotor and ventral striatum were also modulated by probability correct. Across the MTL, activity correlated with the probability of being correct, while the perirhinal cortex and right parahippocampal cortex were modulated by the rate of learning. The activity in the ventral striatum robustly coupled with activity in the MTL during learning, while interactions between the associative striatum and the MTL showed the opposite pattern. These findings suggest dissociable computational roles for different subregions of the striatum and MTL. These subregions interact in distinct ways, perhaps forming functionally integrated networks during the learning of arbitrary associations.
    Cerebral Cortex 03/2011; 21(3):647-58. DOI:10.1093/cercor/bhq144 · 8.67 Impact Factor
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