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Human perceptual and metacognitive decision-making rely on distinct brain networks [1]

['Paolo Di Luzio', 'Center For Studies', 'Research In Cognitive Neuroscience', 'University Of Bologna', 'Cesena', 'Luca Tarasi', 'Juha Silvanto', 'School Of Psychology', 'Faculty Of Health', 'Medical Sciences']

Date: 2022-08 

Perceptual decisions depend on the ability to exploit available sensory information in order to select the most adaptive option from a set of alternatives. Such decisions depend on the perceptual sensitivity of the organism, which is generally accompanied by a corresponding level of certainty about the choice made. Here, by use of corticocortical paired associative transcranial magnetic stimulation protocol (ccPAS) aimed at inducing plastic changes, we shaped perceptual sensitivity and metacognitive ability in a motion discrimination task depending on the targeted network, demonstrating their functional dissociation. Neurostimulation aimed at boosting V5/MT+-to-V1/V2 back-projections enhanced motion sensitivity without impacting metacognition, whereas boosting IPS/LIP-to-V1/V2 back-projections increased metacognitive efficiency without impacting motion sensitivity. This double-dissociation provides causal evidence of distinct networks for perceptual sensitivity and metacognitive ability in humans.

Here, we specifically sought to dissociate the functional role of V5/MT+-to-V1/V2 and IPS/LIP-to-V1/V2 networks in motion perception decisions by means of ccPAS. In line with previous findings [ 44 , 45 ], ccPAS aimed at strengthening V5/MT+-to-V1/V2 back-projections is expected to enhance coherent motion perception. Crucially, assuming IPS/LIP major involvement in decision processes [ 22 ], decision certainty modulations [ 23 ] and choice formation [ 26 , 27 ]; information-based [ 32 ] IPS/LIP-to-V1/V2 ccPAS is expected to drive shifts in choice-related metacognitive awareness, without impacting perceptual sensitivity per se. Conversely, parieto-occipital stimulation lacking STDP specificity should not lead to behavioral modifications.

Yet, the relevance of IPS/LIP in specific aspects of decision confidence [ 23 , 46 ], in association with evidence of back-projections from parietal to early visual areas [ 47 – 49 ] and their possible role in visual awareness [ 50 , 51 ], raises the question about the functional role of these latter parieto-occipital connections in perceptual decision-making. Indeed, a fundamental and yet unanswered question is whether and how do IPS/LIP-to-V1/V2 back-projections functionally contribute to decision-making process, including its confidence.

Visual awareness for global coherent motion (i.e., evidence of movement) has been shown to require the recruitment of feedback pathways from V5/MT+-to-V1/V2 [ 28 , 29 ]. Such connections can be transiently strengthened by means of a novel transcranial magnetic stimulation (TMS) protocol, based on the Hebbian principle, namely the corticocortical paired associative stimulation (ccPAS) [ 30 – 34 ]. This noninvasive stimulation implies a repetitive activation of interconnected cortical sites at specific interstimulus intervals, which are based on the timing of physiological communication between targeted areas, so to mimic patterns of neuronal stimulation shown to induce spike timing–dependent plasticity (STDP)—a form of synaptic plasticity meeting the Hebbian principle that synapses are potentiated if the presynaptic neuron fires immediately before the postsynaptic neuron in a coherent and repeated manner [ 35 – 37 ]. ccPAS has proved capable of modifying neurophysiological responses [ 38 – 41 ] and recently opened the possibility of testing its behavioral consequences [ 42 , 43 ], such as leading to enhanced perceptual discrimination of coherent motion when targeting V5/MT+-to-V1/V2 back-projections [ 44 , 45 ].

Moreover, electrical microstimulation in animals [ 20 ] has confirmed the causal role of V5/MT+ in representing sensory evidence, showing that enhanced perceptual discrimination is possibly driven by signal amplification mechanisms, which may in turn influence confidence generation [ 21 ]. Conversely, other animal studies pointed to the fundamental role of the lateral intraparietal cortex (LIP) in shaping the decision process per se [ 22 ]. Decision certainty modulations have been found during LIP stimulation in monkeys [ 23 ], in line with the notion that this area and the corresponding intraparietal sulcus (IPS) in humans [ 24 , 25 ] are implicated in choice formation [ 26 , 27 ].

From a behavioral perspective, accuracy and confidence in perceptual decision have been frequently dissociated in nonhuman primates [ 6 ] and humans [ 7 – 10 ]. There is empirical evidence of simple dissociations between perceptual sensitivity and metacognitive processes in the form of selective perturbations of confidence without alterations of discriminative performance [ 11 , 12 ]; in fact, the existence of a metacognitive noise has been proposed to describe sources that selectively influence confidence generation, such as previous trials bias [ 13 ], arousal [ 14 ], or fatigue [ 15 ]. Behavioral evidence is further supported by the existence of specific neural correlates, which suggest distinct computations underlying sensory decisions and metacognitive abilities [ 16 , 17 ]. However, it is still unclear whether it is possible to actively induce a targeted modulation of perceptual sensitivity and metacognition by intervening on the efficiency of the cortical networks underlying these components of perceptual decisions.

The ability to exploit available sensory information in order to select the most adaptive option from a set of alternatives represents a fundamental decisional skill. Once a perceptual judgment about a stimulus is made, the resulting subjective belief that the perceptual decision is correct is referred to as confidence. Evaluation of confidence can be intended as a metacognitive process, since it represents a postdecisional outcome regarding the accuracy of first-order choice [ 1 , 2 ]. These components of perceptual decision-making may appear intrinsically intertwined, and yet, recent behavioral and neural findings hint at a possible functional dissociation between performance accuracy and confidence [ 3 – 5 ].

Results and discussion

Fifty-one participants were requested to determine the horizontal direction of a dots pattern in a discrimination task (Fig 1B), in which trials varied across a percentage gradient of motion coherence (i.e., 10 levels from low to high coherence, see Methods), and subsequently rated the confidence on their response (Fig 1A). Sensory discrimination and response certainty were assessed in a between-subjects design before and after the administration of the ccPAS protocol (Fig 1D) over 2 key networks involved in perceptual decision, namely, V5/MT+-to-V1/V2 pathway (i.e., Exp V5-V1 ) and IPS/LIP-to-V1/V2 pathway (i.e., Exp IPS-V1 ), with the relative control condition (i.e., Ctlr IPS-V1 ). Participants underwent the ccPAS procedure following a baseline (BSL) assessment, after which they repeated the initial measure in 2 testing sessions immediately after (T0) and 30 minutes after ccPAS (T30) (see Methods) (Fig 1C).

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TIFF original image Download: Fig 1. Experimental paradigm. (a) Task sequence. Each trial started with a fixation cross-displayed for 500 ms followed by a dot motion stimulus displayed for 400 ms, presented on the right side of the cross. Participants were requested to press a response key immediately after the offset of the stimulus, by selecting the coherent motion perceived (e.g., leftward or rightward) and subsequently to report their confidence by pressing the respective numeric keys (e.g., 1,2,3,4). No time out was present for both responses. (b) Stimuli. The motion coherence of the stimulus varied across trials (ranging from 0% up to 80%, across 10 levels); here a schematic representation of a stimulus with 8% of dots moving rightward. (c) Experiment timeline. For each participant, the experiment began with a training session of 2 blocks, performed to allow the participant to reach a stable performance level before the actual experiment. This preliminary phase was followed by a BSL session. After the BSL measurement, participants were randomly assigned to one of 2 ccPAS conditions. Participants had to perform the same task immediately (T0), and 30 (T30) minutes following the ccPAS protocol. One session consisted of three blocks of 200 trials each. (d) ccPAS protocols. The stimulation lasted 15 minutes and consisted of 90 paired pulses at fixed intensity (60% of TMS max output). The parameters and cortical target varied relative to the pathway involved. In particular, the IPI between stimulated areas was set to 20 ms for Exp V5-V1 , 30 ms for Exp IPS-V1 , and 0 ms for Ctrl IPS-V1 . BSL, baseline; ccPAS, corticocortical paired associative stimulation; IPI, interpulse interval; TMS, transcranial magnetic stimulation. https://doi.org/10.1371/journal.pbio.3001750.g001

Analyses performed on baseline-corrected motion sensitivity threshold (see Fig 2 for group psychometric curves) across the Exp V5-V1 , Exp IPS-V1 , and Ctlr IPS-V1 (i.e., Targeted Network factor) ccPAS conditions depending on the time from stimulation (i.e., Time factor: T0, T30) revealed a significant impact of ccPAS condition (Main effect of Targeted Network: F 2,48 = 6.51; p = .003; np2 = .21) irrespective of the session (Targeted Network*Time: F 2,48 = .27; p = .76; np2 = .01), showing larger improvements following Exp V5-V1 ccPAS relative to Exp IPS-V1 ccPAS (p = .001) and relative to Ctlr IPS-V1 (p = .02) (Fig 3A). Relative to baseline, motion discrimination abilities significantly improved following ccPAS targeting of V5/MT+-to-V1/V2 back-projections, as reflected by a reduction of sensitivity threshold (Exp V5-V1, Avg T0+T30: Mean = −1.85; SEM = .58; p = .02; Cohen’s d = −.77), as expected [44,45]. Crucially, such effect was selective for Exp V5-V1 ccPAS as no significant modulation in perceptual accuracy could be observed following ccPAS targeting the IPS/LIP-to-V1/V2 reentrant pathway (Exp IPS-V1, Avg T0+T30: Mean = .88; SEM = .57; p = .28; Cohen’s d = .38) or the IPS/LIP-V1/V2 network (Ctrl IPS-V1, Avg T0+T30: Mean = −.01; SEM = .48; p = .97; Cohen’s d = −.008), thus confirming the causal role of the V5/MT+-to-V1/V2 pathway in global motion sensitivity and showing its anatomical specificity. These results were corroborated by a Bayesian analysis, revealing that the model including the ccPAS condition (i.e., the Targeted Network factor) better predicts performance (BF inclusion = 14.99) relative to models excluding it, and data about motion sensitivity of Exp V5-V1 consistently support the hypothesis of the improvement (BF 10 = 8.55) relative to Exp IPS-V1 (BF 10 = .69) and Ctrl IPS-V1 (BF 10 = .25). Additional analysis on raw behavioral measures have also been reported on Supporting information (S1 File) along with additional plots (S1–S3 and S4 Figs) further detailing the nature of these effects.

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TIFF original image Download: Fig 2. Psychometric curves. Fitted data modeled on the logistic function to obtain the perceptual thresholds of motion discrimination. Group performance are separately plotted depending on the type of stimulation (top graph, in red Exp V5-V1 ; mid graph, in blue Exp IPS-V1 ; bottom graph, in yellow Ctrl IPS-V1 ) and as a function of the session. Gray dots depict the perceptual threshold coincident with the percentage of coherent motion where the logistic function had a value of 75% of correct responses. Perceptual thresholds shifts on the abscissa represent lower (right-shift) or higher (left-shift) motion sensitivity. Data underlying this figure can be found in OSF: https://osf.io/x7d2e/?view_only=ac2ff19b1ab6415cb471895854fb5a35. https://doi.org/10.1371/journal.pbio.3001750.g002

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TIFF original image Download: Fig 3. ccPAS effect on decision-making. (a) Motion threshold following stimulation. Filled bars represent the mean change Δ in sensitivity threshold (e.g., differences between Post ccPAS and BSL), and error bars represent the SEM. Individual data points are plotted by scattered dots. Asterisks point out significance (*p < .05) for Exp V5-V1 mean and between group means. (b) Metacognitive efficiency following stimulation. Filled bars represent the mean change Δ in metacognition with error bars representing SEM. Individual performances are plotted by scattered data points. Asterisks point out significance (*p < .05) for Exp IPS-V1 mean and between group means. Data underlying this figure can be found in OSF: https://osf.io/x7d2e/?view_only=ac2ff19b1ab6415cb471895854fb5a35. BSL, baseline; ccPAS, corticocortical paired associative transcranial magnetic stimulation protocol. https://doi.org/10.1371/journal.pbio.3001750.g003

The impact of ccPAS over V5/MT+-to-V1/V2 and IPS/LIP-to-V1/V2 networks was then tested on metacognitive efficiency, indexed by the matching between confidence attribution and perceptual sensitivity (i.e., difference between meta-d’ and d’; see Methods) at participant’s threshold levels. Modulation of this metacognitive index was again dependent on the ccPAS condition (Main effect of Targeted Network: F 2,48 = 3.29; p = .046; np2 = .12), with larger improvements in metacognition abilities in the Exp IPS-V1 relative to the Exp V5-V1 (p = .03) and relative to Ctlr IPS-V1 (p = .04) conditions, independently of session (Targeted Network*Time: F 2,48 = .03; p = .97; np2 = .001). Participants showed increased metacognition following ccPAS targeting the IPS/LIP-to-V1/V2 pathway (Exp IPS-V1, Avg T0+T30: Mean = .46; SEM = .14; p = .01; Cohen’s d = .79) relative to baseline. No modulation in metacognitive efficiency was observed following ccPAS targeting the V5/MT+-to-V1/V2 network (Exp V5-V1, Avg T0+T30: Mean = −.02; SEM = .14; p = .89; Cohen’s d = −.03) or nonspecific stimulation of the parieto-occipital network (AVG T0+T30: Mean = .02; SEM = .16; p = 1; Cohen’s d = .04) (Fig 3B). Consistently, Bayesian ANOVA confirmed that metacognitive data were adequately explained (BF inclusion = 1.79) by a model including the ccPAS condition (i.e., Targeted Network), supporting a metacognition improvement in Exp IPS-V1 (BF 10 = 11.16), but not in Exp V5-V1 (BF 10 = .25) or Ctrl IPS-V1 (BF 10 = .25). Supplementary analysis on metacognition and raw confidence data, with related plots, have been reported separately (S5 and S6 Figs), further detailing the nature of these effects. Briefly, additional analyses on raw data highlight a different impact of the stimulation group on confidence rating for correct and error responses. Specifically, we found that following IPS/LIP-to-V1/V2 ccPAS, participants confidence increased exclusively for correct trials (t = 2.87; p = .04) with no alteration for error trials (t = 1.65; p = .12). In contrast, following V5/MT+-to-V1/V2 ccPAS, participants showed a general increase in confidence, independently of whether their responses were correct (t = 3.62; p = .01) or incorrect (t = 3.29; p = .02), speaking in favor of a specific role of IPS-V1 back-projections in sensory processing readout (S6 Fig).

Here, we showed that distinct visual networks can be functionally dissociated when investigating metacognitive functions, complementarily to perceptual discrimination performance. These effects cannot be alternatively explained by simple time passing—which in principle might have made participants more efficient at rating their confidence over time—or any unspecific effect of TMS. Nonspecific stimulation of the parieto-occipital stream (Ctrl IPS-V1 ) showed no modulatory effects in terms of motion sensitivity or metacognitive functions. Moreover, prior work using the same motion task has shown no change in perceptual sensitivity following sham or ineffective stimulation of the V5/MT+-to-V1/V2 network [44,45].

Our findings provide causal evidence of a double dissociation of functional networks orchestrating perceptual decision-making in humans, namely, V5/MT+-to-V1/V2, accounting for visual motion discrimination sensitivity, and IPS/LIP-to-V1/V2, accounting for accurate confidence judgments. In line with current opinions [3,52] that sensitivity and confidence could be served by partially distinct processes, we reported for the first time that the TMS protocol aimed at enhancing IPS/LIP-to-V1/V2 pathway selectively affects metacognitive capacity in a functional way, with participants becoming effectively more accurate in estimating the quality of their choices (i.e., more accurate in their confidence ratings).

Crucially, we found evidence of a functional segregation of targeted networks. The enhanced metacognitive capacity did not lead to simultaneous increase of motion sensitivity, being this a function subserved by another network. Indeed, ccPAS over V5/MT+-to-V1/V2 back-projections was critical in increasing motion sensitivity and accuracy, as expected [44,45].

These findings challenge the view that higher perceptual accuracy, as the one induced by ccPAS over V5/MT+-to-V1/V2 back-projections, may produce a modulation of metacognitive functions due to a finer discrimination of the stimuli, as assumed by a model where perceptual decision and confidence are based on a common underlying neural representation [21,53]. This interpretation would not explain why ccPAS over V5/MT+-to-V1/V2 back-projections does not lead to enhanced metacognitive efficiency. Instead, it supports the notion that confidence generation and perceptual sensitivity are supported by relatively independent mechanisms [54–56]. In detail, the sensory representation necessary for the perceptual readout would not be the absolute source for metacognitive estimation, being the latter the result of an accumulation process, which integrates further information after, or even while the perceptual choice is made [16,57]. This mechanism would admit conditions in which alterations of sensory representation produce divergences between perceptual and metacognitive outcomes [7,58], and seems to be suggested by secondary evidence showing a bias in confidence generation following V5/MT+-to-V1/V2 stimulation (see Text B in S1 File), leading the subjects to nonspecific overestimation of certainty, without altering their metacognitive efficiency (Text C in S1 File).

On the other hand, neurostimulation aimed at enhancing the IPS/LIP-to-V1/V2 back- connectivity improved metacognitive ability without impacting motion sensitivity. This effect may be possibly sustained by an optimized performance to confidence degree mapping (Text B and C in S1 File). Consistently to what had already been demonstrated for the V5/MT+-to-V1/V2 network [45,46], here, the effect was conditional to the causal order of the pulses, since no outcome could be observed when controlling for timing (Ctrl IPS-V1 ). This result, taken together with previous findings reporting the selective manipulations of confidence without affecting accuracy [7,16,59,60], is in line with the proposal that considers metacognition as a distinct functional process [2,59,61]. This implies a system where the actual computations that underlie these 2 processes may be sustained by dissociable, perhaps both in time and spatial scale, neural circuits [57]. Given this, it is crucial to address what could be a plausible neural mechanism for the overall pattern of results. Assuming distinct elaboration levels for perceptual decision and confidence, the activity emerging from V5/MT+-to-V1/V2 network appears fundamental for sensory discrimination. This reentrant pathway subserves an adaptive mechanism that adjusts local circuitry of V1 to highlight output of cells representing salient information and suppress others irrelevant information [62], thus optimizing representation of the predicted trajectory in MT+/V5 to overcome direction uncertainty, and improving the final readout. As previously mentioned, the sensory evidence is then plausibly involved in the transformations needed for metacognitive estimation; however, this step incorporates other sources, identified as metacognitive noise [63], leading to a distinct representation. We propose that the improved metacognitive performance following IPS/LIP-to-V1/V2 stimulation may be a consequence of decreasing noise in confidence generation, as already suggested in other studies with neuromodulation on metacognition [55,64]. In this case, reduction of metacognitive noise could derive from an efficient gating of early visual areas (V1-V2) from parietal area (IPS/LIP) by back-projections, possibly orchestrating neuronal firing with a fine balance between excitation and inhibition [65]. The suggested process would reduce the uncertainty estimates in the circuit for metacognitive computation by stabilizing the neural activity in early visual cortex. This function is not at odds with the alpha frequency-specific activity attributed to feedback influence [66,67], mediating inhibitory and disinhibitory effects on visual areas [68–71]. Consistently with the hypothesis of distinct functional computations for accuracy and confidence, the abovementioned mechanism would selectively shape the representation of confidence without affecting the first-order representation used for sensory discrimination, possibly tuning specific oscillatory parameters.

Interestingly, a recent preprint supports the critical involvement of alpha oscillations in feedback activity by showing an association between boosting V5/MT+-to-V1/V2 connectivity and alpha modulation [72]. These findings are very intriguing for the current report in the light of recent evidence for the role of different parameters of alpha oscillations in generating perceptual sensitivity versus confidence and metacognitive functions [5]. Importantly, metacognitive abilities have been shown to correlate with modulation in alpha amplitude only following stimulus presentation, in line with the idea of poststimulus choice metacognitive readout.

By taking into account the evidence that early visual areas and higher-order regions constitute a recurrent feedback system [73], we could also hypothesize the existence of a hierarchical Bayesian architecture in which looping iterations tend to perform near-optimal computations [74,75], combining and updating predicted and observed input to reduce uncertainty. Empirically, it has been reported that in recurrent circuit models of decision-making, reentrant pathways continuously propagate the evolving decision variable from upstream regions to sensory regions [76,77], and the state of the early visual cortex is shaped by an adaptive, stabilizing feedback of the evolving decision variable [78,79]. In a related line of reasoning, the parietal node may serve a higher-order supervisory function feeding back lower-level areas and thus integrating recursive information across the hierarchy. For example, comparing the expected sensory signal as computed in V5/MT+ (motion direction) with the effective signal update recorded in early visual areas (actual stimulus position) may provide a near-optimal mechanism modulating confidence levels depending on the match between expected and actual sensory signal in V1/V2. Small differences between expected and actual sensory signal computation prompt maximum confidence and vice versa. Recursive cycles between IPS/LIP and V1/V2 would then promote the metacognitive awareness associated with the task.

It should be noted that a previous attempt of active manipulation in posterior parietal cortices by means of TMS failed to trace any effect on metacognitive functionality [80]. This outcome was presumably due to a different cortical site location and a distinct stimulation paradigm employed relative to ours. Nevertheless, the potential of TMS at dissociating choice component of accuracy and confidence has been proven extensively in other works, mainly involving the causal manipulation of the prefrontal cortex [11,81] and early visual areas [4,82]. Here, we provide the first evidence of a causal involvement of the functional pathway from parietal to early visual areas in metacognitive processes. In light of these results, we also consider reasonable that an increased functionality of the parieto-occipital stream at integrating perceptual information might favor the metacognitive readout mechanism that occurs from the communication between frontal (e.g., BA10) and parietal (e.g. LIP/IPS) regions [83]. This seems a plausible explanation given the existence of a series of recursive chains that are diffused along the frontoparietal axis [84,85]; moreover, it appears in line the notion of a long-range distributed network involved in metacognition [57,86]. Yet, regardless of the extension of the specific brain network involved, our findings support a critical role for IPS-to-V1/V2, rather than V5/MT+-to-V1/V2 pathways in visual metacognition.

In conclusion, we functionally dissociate the role of V5/MT+-to-V1/V2 and IPS/LIP-to-V1/V2 back-projections in perceptual decision processes. Our findings provide evidence supporting a selective modulation of perceptual sensitivity through signal amplification by V5/MT+-to-V1/V2 back-projections and metacognitive efficiency through uncertainty supervision by IPS/LIP-to-V1/V2 back-projections speaking in favor of distinct but integrated systems subserving near-optimal perceptual decision processes in humans.

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