Striatal activation as a neural link between cognitive and perceptual flexibility
Introduction
Adaptive behavior requires both flexibility and stability in the perceptual and in the cognitive domain. Our perception of the world is usually experienced as unique and stable even though the sensory data are often noisy. At the same time, our sensory systems continuously ‘evaluate’ different interpretations in order to enable flexible updates of conscious experience. A compelling example of this perceptual flexibility are ambiguous stimuli that are compatible with two perceptual interpretations (Leopold and Logothetis, 1999, Sterzer et al., 2009). For example, during viewing of ambiguous visual stimuli like the Necker Cube, perception keeps switching between two stable, mutually exclusive interpretations, a phenomenon commonly referred to as bistable perception. The rate of such perceptual switching, which is rather stable within individuals (George, 1936, Pettigrew and Miller, 1998) but highly variable between individuals (Kleinschmidt et al., 2012), can be regarded as a measure of an individual's flexibility in updating perception. Individual differences in perceptual switch rates have been related to genetic factors, especially those associated with dopaminergic neurotransmission (Miller et al., 2010, Kondo et al., 2012, Shannon et al., 2011, Schmack et al., 2013). Neurally, perceptual switching is thought to involve local processes in visual cortex, such as adaptation and mutual inhibition between neuronal populations (Blake and Logothetis, 2002, Sterzer et al., 2009). In addition, there is evidence that brain regions that have been implicated in cognitive control processes, e.g. in fronto-parietal cortices, mediate switches during bistable perception, thus suggesting a role for non-sensory brain circuits in perceptual flexibility (Leopold and Logothetis, 1999, Sterzer et al., 2009).
Similar to the perceptual domain, there is also considerable individual variability in tasks that require cognitive flexibility (e.g., Stelzel et al., 2010, Herd et al., 2014, Armbruster et al., 2012, Braver, 2012). Cognitive flexibility comprises endogenous control over currently active goals and the updating of task-relevant information in the context of changing environmental demands (Monsell, 2003). Neural correlates of cognitive flexibility have been ascribed to lateral frontoparietal regions (Derrfuss et al., 2005, Badre and D'Esposito, 2009), similar to the regions implicated in bistable perception (Sterzer et al., 2009). In addition, dopamine-dependent signals from striatal regions have been associated with the process of switching between two cognitive states that either facilitate flexible updating of representations or promote cognitive stability (Frank et al., 2001, Durstewitz and Seamans, 2008, Stelzel et al., 2010, Stelzel et al., 2013, Cools and D'Esposito, 2011).
Given the anatomical and neurochemical similarities with regard to perceptual and cognitive flexibility, we here probed whether individual differences in perceptual flexibility during bistable perception are related to individual cognitive flexibility and associated neural correlates. In a behavioral experiment we assessed perceptual switch rates during viewing of Necker cube lattice as a measure of perceptual flexibility (Fig. 1b). In order to assess cognitive flexibility, participants performed rule-based task switching during functional magnetic resonance imaging (fMRI). Given the outlined overlap in the neural mechanisms of perceptual and cognitive flexibility, we hypothesized to find a link between switch rates in bistable perception and both fMRI signals as well as behavioral measures associated with rule-based task switching.
Section snippets
Participants
126 healthy, right-handed individuals with normal or corrected-to-normal vision participated in the study; one participant was excluded from the analysis due to a psychiatric condition. Because of technical problems in data collection and analysis we excluded 9 participants from the analysis of the task-switching paradigm, leaving 117 participants (age 26.16 ± 3.78, 61 females). 112 individuals (age 26.19 ± 3.75, 60 females) participated in the bistable perception experiment; 4 additional
Task switching
As shown previously, switching between tasks compared to task repetitions involved performance costs shown by increased mean response times (RT) (88.69 ± 5.21 ms, SEM; t(116) = − 17.03, p < 0.001) and error rates (4.13 ± 0.52%, SEM; t(116) = − 7.96, p < 0.001). Additionally both conditions revealed a significant difference in inverse efficiency, a measure of mean RTs corrected by the accuracy (136.38 ± 2.8 ms, SEM; t(116) = − 15.73, p < 0.001. As error rates were generally rather low (range: 4.66 to 8.79%), reaction
Discussion
We provide first evidence for an association between individual differences in perceptual and cognitive flexibility. Individuals with shorter phase durations during the perception of an ambiguous figure (and thus higher perceptual flexibility) showed decreased task-switching-related activity in the basal ganglia centered around the right putamen and although weaker lower task-switching costs (RT) (and thus higher cognitive flexibility) behaviorally.
These findings have important implications for
Conclusion
To summarize, the present results provide evidence that individual differences in cognitive flexibility and associated fronto-striatal processing contribute to differences in perceptual flexibility. Although future studies are needed to deepen the understanding of this relationship, our findings form the basis for a more general framework of bistable perception and extend our current knowledge concerning the relationship between perception and cognitive control.
Conflict of interest
The authors declare no competing financial interests.
Acknowledgement
This work was supported by the Berlin School of Mind and Brain and Deutsche Forschungsgemeinschaft (Collaborative Research Centre “Volition and Cognitive Control”, DFG grant SFB 940/1 2013), Technical University Dresden; DFG grant STE 1430/7-1).
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