Perceptual metacognition of human faces is causally supported by function of the lateral prefrontal cortex

Metacognitive awareness—the ability to know that one is having a particular experience—is thought to guide optimal behavior, but its neural bases continue to be the subject of vigorous debate. Prior work has identified correlations between perceptual metacognitive ability and the structure and function of lateral prefrontal cortex (LPFC); however, evidence for a causal role of this region in promoting metacognition is controversial. Moreover, whether LPFC function promotes metacognitive awareness of perceptual and emotional features of complex, yet ubiquitous face stimuli is unknown. Here, using model-based analyses following a causal intervention to LPFC in humans, we demonstrate that LPFC function promotes metacognitive awareness of the orientation of faces—although not of their emotional expressions. Collectively, these data support the causal involvement of the prefrontal cortex in metacognitive awareness, and indicate that the role of LPFC in metacognition encompasses perceptual experiences of naturalistic social stimuli.


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Behavioural & social sciences study design
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Study description
The data are experimental (within-subjects design) and quantitative.

Research sample
We recruited thirty-four right-handed individuals from the University of Wisconsin-Madison between the ages of 18-35 y who had been previously screened in a clinical interview for neurological and psychiatric conditions, as well as for TMS and MRI safety criteria. One participant did not tolerate TMS delivered to the LPFC target, therefore rendering the maximum sample size N = 33 (19 males; age 18-32; M = 23.79, SD = 4.428). The sample is representative of the required healthy sample for TMS+MRI studies.

Sampling strategy
Sampling was random. The sample size for the present study was determined based on a power analysis performed on data from the most pertinent published experiment probing the causal role of LPFC function on visual metacognition via cTBS that was available at the time of participant recruitment (Rounis et al. 2010). In their study, statistical power obtained for the paired-mean difference of metacognitive awareness sensitivity following cTBS to LPFC vs. sham was d = 0.693, which required a sample size of n = 19 to detect a statistically significant effect at alpha two-tailed p < .05 and power = 80%.Therefore, with the goal of retaining a minimum of n = 19 participants with usable data across the multiple (n = 2) TMS sessions and (n = 4) psychophysical assessments, we recruited thirty-four right-handed individuals from the University of Wisconsin-Madison.

Data collection
Prior to behavioral data collection, a high resolution MRI was collected from the participants to allow for accurate neuronavigation.
During behavioral data collection, participants sat at with their eyes positioned 80cm away from the computer monitor (ASUS HDMI set to 60Hz refresh rate; 53cm screen width; 1920 x 1080 pixels resolution). At least n=2 researchers were present during TMS administration and data collection (RCL and one or more undergraduate research assistants). The experiment was single blind (RCL was not blind to the experimental hypothesis; undergraduate research assistants were).
TMS was delivered to the left LPFC and to medial S1 with a Magstim Super Rapid magnetic stimulator (Magstim, Whitland, UK) equipped with a figure-8 stimulating coil. Precise TMS targeting on a subject-by-subject basis was achieved via a Navigated Brain Stimulation (NBS) system (Nextstim, Helsinki, Finland), which uses infrared-based frameless stereotaxy to map the position of the coil and the subject's head in relation to the space of the individual's high-resolution MRI. In order to temporarily interfere with function of LPFC and Control/ S1 sites, we used a continuous TMS protocol-cTBS-consisting of 50Hz trains of 3 TMS pulses repeated every 200 ms continuously over a period of 20 seconds (300 pulses total). As is typical with this TMS protocol, we delivered cTBS at 80% of active motor threshold.

Timing
Start date: December 2014. End date: May 2015.

Data exclusions
We used the method of constant stimuli to determine psychophysical performance and estimate metacognition for near-threshold stimuli (as per prior work and a primary goal of the present manuscript), as well as to examine the potential role of LPFC in promoting metacognition outside of the near-threshold range. We report in the main manuscript analysis of participants whose data allowed for the appropriate estimation of their stimulus detection threshold for each metacognition task, as detailed next. For the face orientation task, n=28 (out of 33) participants' stimulus-detection threshold fell within the contrast range spanned by the stimuli used in the method of constant stimuli; those participants were therefore included in the analysis (n=5 participants were at ceiling; final sample: 16 males; age 18-32; M = 23.5, SD = 4.718). In the emotional-expression discrimination task, n=32 (out of 33) met this criterion (

Randomization
The design is within-subjects--all subjects underwent all experimental conditions. Assignment to "LPFC site first" vs. "S1 site first" was based on subject number (odd or even). Assignment of whether awareness task of face orientation vs. face emotion was tested first was based on session number in an orthogonal manner to the TMS site order assignment (where awareness task order alternated every n=4 sessions).
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