Neurochemical and functional interactions for improved perceptual decisions through training

Abstract

Learning and experience are known to improve our ability to make perceptual decisions. Yet, our understanding of the brain mechanisms that support improved perceptual decisions through training remains limited. Here, we test the neurochemical and functional interactions that support learning for perceptual decisions in the context of an orientation identification task. Using magnetic resonance spectroscopy (MRS), we measure neurotransmitters (i.e., glutamate, GABA) that are known to be involved in visual processing and learning in sensory [early visual cortex (EV)] and decision-related [dorsolateral prefrontal cortex (DLPFC)] brain regions. Using resting-state functional magnetic resonance imaging (rs-fMRI), we test for functional interactions between these regions that relate to decision processes. We demonstrate that training improves perceptual judgments (i.e., orientation identification), as indicated by faster rates of evidence accumulation after training. These learning-dependent changes in decision processes relate to lower EV glutamate levels and EV-DLPFC connectivity, suggesting that glutamatergic excitation and functional interactions between visual and dorsolateral prefrontal cortex facilitate perceptual decisions. Further, anodal transcranial direct current stimulation (tDCS) in EV impairs learning, suggesting a direct link between visual cortex excitation and perceptual decisions. Our findings advance our understanding of the role of learning in perceptual decision making, suggesting that glutamatergic excitation for efficient sensory processing and functional interactions between sensory and decision-related regions support improved perceptual decisions.NEW & NOTEWORTHY Combining multimodal brain imaging [magnetic resonance spectroscopy (MRS), functional connectivity] with interventions [transcranial direct current stimulation (tDCS)], we demonstrate that glutamatergic excitation and functional interactions between sensory (visual) and decision-related (dorsolateral prefrontal cortex) areas support our ability to optimize perceptual decisions through training.

Keywords: MR spectroscopy; functional connectivity; learning; perceptual decisions; transcranial direct current stimulation.

Graphical abstract

Figure 1.

Behavioral task and performance. A: orientation identification task. Participants judged the orientation of a Gabor patch presented (45° or 135°) among Gaussian noise patterns. B: mean performance across participants for the pretest (Pre) and training (tr1–tr5) blocks. C and D: mean drift rate (C) and threshold (D) derived from diffusion modeling [drift rate, decision threshold, nondecision time (DR-TH-Ter) model] across participants for the pretest and training blocks. Error bars indicate SE across participants. We used the Bayesian information criterion (BIC) for 5 constructed models and selected the DR-TH-Ter model with the lower BIC value (i.e., null model: 3,246.22, DR model: 3,267.02, DR-TH model: 3,234.13, DR-TH-Ter model: 3,228.73, full model: 3,308.36).

Figure 2.

Relationship of magnetic resonance spectroscopy (MRS) glutamate and GABA+ to behavior. A: MRS voxels and spectra in the early visual cortex (EV) and dorsolateral prefrontal cortex (DLPFC). We illustrate a group MRS mask (sagittal, axial view) that covers a cortical area that is common in at least 50% of the participants’ MRS voxels (red, EV; yellow, DLPFC). Sample spectra from the MRS voxels show the LCModel fit, residual, and respective fits for GABA+, glutamate (Glu), glutamine, glutathione, and N-acetylaspartate (NAA). B: multiple regression of EV Glu with behavior: significant negative linear relationship with drift rate (DR) but not decision threshold (TH) change (max-training block minus pretraining block). C: no significant linear relationship of EV GABA+ with behavior. D: no significant linear relationship of DLPFC Glu with behavior. E: no significant linear relationship of DLPFC GABA+ with behavior. Significant results are indicated by filled symbols and nonsignificant results by open symbols.

Figure 3.

Relationship of early visual cortex (EV)-dorsolateral prefrontal cortex (DLPFC) functional connectivity to behavior and glutamate (Glu). EV-DLPFC functional connectivity (Fisher’s z), as measured by resting-state functional magnetic resonance imaging (rs-fMRI), shows a significant negative linear relationship with drift rate (DR) but not decision threshold (TH) change (multiple regression) (A), a significant positive linear relationship with EV Glu but not EV GABA+ (B), and no significant linear relationship with DLPFC Glu or GABA+ (C). Significant results are indicated by filled symbols and nonsignificant results by open symbols.

Figure 4.

Transcranial direct current stimulation (tDCS) intervention: mean accuracy (A), drift rate (B), and decision threshold (C) across participants in the Anodal and Sham groups for the pretest (Pre) and max-training (Max) blocks. Error bars indicate SE across participants. Open circles indicate individual participant data.