Using PIDs to map the flow of task-relevant information from human brain measurements in a perceptual decision-making task
Hamed Nili, Marco Celotto, Alessandro Toso, Tobias Donner, and Stefano Panzeri
How can we reverse engineer the information flow within the brain that leads humans to take appropriate decisions based on the available sensory evidence? Recordings of brain activity of subjects performing perceptual discrimination tasks have begun to reveal qualitatively the distribution across brain areas and frequency bands of neural signals encoding the sensory stimulus or the subject’s decision (Wilming et al., Nat. Commun. 2020), as well as mapping the transmission of activity between selected pairs of visual regions (Bosman et al., Neuron 2012; Ferro et al., PNAS 2021). Despite this progress, we still lack a quantitative framework to map the information processing underlying perceptual decision making.
In this work, we develop this framework using Partial Information Decompositions (PID). We also demonstrate its power to reveal such computations in large brain networks recorded from the human brain. Specifically, our objective is to perform a complete identification of when and how sensory information is encoded in the cortical hierarchy and in the frequency activity space, how it is transmitted to other brain areas, and how is used to guide behavioral choice.
We analysed published whole-brain MEG recordings (Wilming et al., Nat. Commun. 2020) from human participants performing a visual contrast discrimination task entailing a sequence of 10 discrete sample stimuli whose contrast had to be averaged and compared to a reference. We used mutual information to quantify stimulus and choice information in brain activity across time, frequency, and 180 regions per hemisphere covering the entire cortex. We used Intersection Information (II, Pica et al., NIPS 2017), which is based on PID, to quantify how much of the sensory information encoded in neural activity is used to inform choices. Additionally, using the same framework, we quantified the extent to which stimulus or choice information are redundant/synergistic in the homotopic ROIs. Moreover, we measured the amount of information about stimulus or choice transmitted between cortical areas using our newly developed Feature-specific Information Transfer (FIT) measure (Bim et al., BioRxiv, 2020)
We identified frequency bands that carried stimulus, choice, and intersection information across cortex. Stimulus information used to inform choices was initially carried in the gamma-band, [40, 80) Hz, in visual, parietal and posterior cingulate regions. Choice signals later developed in the alpha-/beta-bands, [8, 40) Hz, in downstream regions of premotor and somato-motor cortex. The region-specific time-frequency patterns of information had distinguishable profiles for different anatomical groups and among the different measures, intersection information provided the highest level of discriminability. We also found that the pattern of redundancy/synergy of information in homotopic ROIs (i.e., across the left and right hemispheres) was different across regions, frequency bands and was content-dependent. Stimulus information was encoded redundantly between left and right homotopic ROIs in visual areas and gamma frequency band. Choice information was encoded synergistically across the two hemispheres in downstream areas and in lower frequencies. In some areas, like the Parietal cortex, both patterns were present. Investigating information transfer across regions, we found that stimulus-specific and choice-specific information were broadly transmitted across many areas. The transmission of stimulus information occurred predominantly in the feedforward direction in the gamma-band, and transmission of choice information predominantly in the feedback direction in the alpha-/beta-bands.
In sum, using information theory, we mapped the encoding and transmission of task-relevant variables across frequency and cortical locations in the human brain during a perceptual discrimination task. This revealed a transformation over time of stimulus information in the gamma band in visual, parietal and cingulate areas into choice signals in the beta and alpha band in downstream areas, mediated by distributed patterns of feedforward gamma stimulus information and feedback alpha-beta choice information transmission.
References
Wilming, N., Murphy, P. R., Meyniel, F., & Donner, T. H. (2020). Large-scale dynamics of perceptual decision information across human cortex. Nature communications, 11(1), 5109.
Bosman, C. A., Schoffelen, J. M., Brunet, N., Oostenveld, R., Bastos, A. M., Womelsdorf, T., ... & Fries, P. (2012). Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron, 75(5), 875-888.
Ferro, D., van Kempen, J., Boyd, M., Panzeri, S., & Thiele, A. (2021). Directed information exchange between cortical layers in macaque V1 and V4 and its modulation by selective attention. Proceedings of the National Academy of Sciences, 118(12), e2022097118.
Pica, G., Piasini, E., Safaai, H., Runyan, C., Harvey, C., Diamond, M., ... & Panzeri, S. (2017). Quantifying how much sensory information in a neural code is relevant for behavior. Adv. Neural Inf. Process. Syst. (NeurIPS) 30: 3686–3696.
Bím, J., De Feo, V., Chicharro, D., Hanganu-Opatz, I. L., Brovelli, A., & Panzeri, S. (2020) A Non-negative Measure Of Feature-specific Information Transfer Between Neural Signals. BioRxiv