Rafael Hernan Polania

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Polania

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Rafael Hernan

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0000-0002-6176-6806

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Publications 1 - 10 of 33

Functional network dynamics between the anterior thalamus and the cortex in deep brain stimulation for epilepsy
Aiello, Giovanna; Ledergerber, Debora; Dubcek, Tena; et al. (2023)
Brain: A Journal of Neurology
Owing to its unique connectivity profile with cortical brain regions, and its suggested role in the subcortical propagation of seizures, the anterior nucleus of the thalamus (ANT) has been proposed as a key deep brain stimulation (DBS) target in drug-resistant epilepsy. However, the spatio-temporal interaction dynamics of this brain structure, and the functional mechanisms underlying ANT DBS in epilepsy remain unknown. Here, we study how the ANT interacts with the neocortex in vivo in humans and provide a detailed neurofunctional characterization of mechanisms underlying the effectiveness of ANT DBS, aiming at defining intraoperative neural biomarkers of responsiveness to therapy, assessed at 6 months post-implantation as the reduction in seizure frequency. A cohort of 15 patients with drug-resistant epilepsy (n = 6 males, age = 41.6 ± 13.79 years) underwent bilateral ANT DBS implantation. Using intraoperative cortical and ANT simultaneous electrophysiological recordings, we found that the ANT is characterized by high amplitude θ (4–8 Hz) oscillations, mostly in its superior part. The strongest functional connectivity between the ANT and the scalp EEG was also found in the θ band in ipsilateral centro-frontal regions. Upon intraoperative stimulation in the ANT, we found a decrease in higher EEG frequencies (20–70 Hz) and a generalized increase in scalp-to-scalp connectivity. Crucially, we observed that responders to ANT DBS treatment were characterized by higher EEG θ oscillations, higher θ power in the ANT, and stronger ANT-to-scalp θ connectivity, highlighting the crucial role of θ oscillations in the dynamical network characterization of these structures. Our study provides a comprehensive characterization of the interaction dynamic between the ANT and the cortex, delivering crucial information to optimize and predict clinical DBS response in patients with drug-resistant epilepsy.
Efficient sampling and noisy decisions
Heng, Joseph A.; Woodford, Michael; Polania, Rafael Hernan (2020)
eLife
Human decisions are based on finite information, which makes them inherently imprecise. But what determines the degree of such imprecision? Here, we develop an efficient coding framework for higher-level cognitive processes in which information is represented by a finite number of discrete samples. We characterize the sampling process that maximizes perceptual accuracy or fitness under the often-adopted assumption that full adaptation to an environmental distribution is possible, and show how the optimal process differs when detailed information about the current contextual distribution is costly. We tested this theory on a numerosity discrimination task, and found that humans efficiently adapt to contextual distributions, but in the way predicted by the model in which people must economize on environmental information. Thus, understanding decision behavior requires that we account for biological restrictions on information coding, challenging the often-adopted assumption of precise prior knowledge in higher-level decision systems.
Rational inattention in mice
Grujic, Nikola; Brus, Jeroen; Burdakov, Denis; et al. (2022)
Science Advances
Behavior exhibited by humans and other organisms is generally inconsistent and biased and, thus, is often labeled irrational. However, the origins of this seemingly suboptimal behavior remain elusive. We developed a behavioral task and normative framework to reveal how organisms should allocate their limited processing resources such that sensory precision and its related metabolic investment are balanced to guarantee maximal utility. We found that mice act as rational inattentive agents by adaptively allocating their sensory resources in a way that maximizes reward consumption in previously unexperienced stimulus-reward association environments. Unexpectedly, perception of commonly occurring stimuli was relatively imprecise; however, this apparent statistical fallacy implies "awareness" and efficient adaptation to their neurocognitive limitations. Arousal systems carry reward distribution information of sensory signals, and distributional reinforcement learning mechanisms regulate sensory precision via top-down normalization. These findings reveal how organisms efficiently perceive and adapt to previously unexperienced environmental contexts within the constraints imposed by neurobiology.
Using an active phase cancellation and multipair design for in-vivo focal temporal interference electrical brain stimulation
Savvateev, Iurii; Missey, Florian; Beliaeva, Valeriia; et al. (2023)
Temporal Interference Stimulation (TI) (1) represents a novel technique for deep brain stimulation, aiming to integrate the depth characteristic of conventional deep brain stimulation protocols with the non-invasive nature of transcranial electric and magnetic stimulations (tACS and TMS). Recent publications in both mice and humans explicitly demonstrated that deep brain areas including the hippocampus and the striatum could be stimulated using TI (2, 3). However, whereas TI stimulation is set to be focused on a specific region of interest (ROI), other off-target areas may still be stimulated due to the field propagation. This is a major concern when TI is employed at high stimulation amplitudes, as off-target stimulations have a potential to cause unwanted side effects such as epileptic convulsions (2).
Toward integrative approaches to study the causal role of neural oscillations via transcranial electrical stimulation
Beliaeva, Valeriia; Savvateev, Iurii; Zerbi, Valerio; et al. (2021)
Nature Communications
Diverse transcranial electrical stimulation (tES) techniques have recently been developed to elucidate the role of neural oscillations, but critically, it remains questionable whether neural entrainment genuinely occurs and is causally related to the resulting behavior. Here, we provide a perspective on an emerging integrative research program across systems, species, theoretical and experimental frameworks to elucidate the potential of tES to induce neural entrainment. We argue that such an integrative agenda is a requirement to establish tES as a tool to test the causal role of neural oscillations and highlight critical issues that should be considered when adopting a translational approach.
Causal contributions of human frontal eye fields to distinct aspects of decision formation
Murd, Carolina; Moisa, Marius; Grueschow, Marcus; et al. (2020)
Scientific Reports
Several theories propose that perceptual decision making depends on the gradual accumulation of information that provides evidence in favour of one of the choice-options. The outcome of this temporally extended integration process is thought to be categorized into the ‘winning’ and ‘losing’ choice-options for action. Neural correlates of corresponding decision formation processes have been observed in various frontal and parietal brain areas, among them the frontal eye-fields (FEF). However, the specific functional role of the FEFs is debated. Recent studies in humans and rodents provide conflicting accounts, proposing that the FEF either accumulate the choice-relevant information or categorize the outcome of such evidence integration into discrete actions. Here, we used transcranial magnetic stimulation (TMS) on humans to interfere with either left or right FEF activity during different timepoints of perceptual decision-formation. Stimulation of either FEF affected performance only when delivered during information integration but not during subsequent categorical choice. However, the patterns of behavioural changes suggest that the left-FEF contributes to general evidence integration, whereas right-FEF may direct spatial attention to the contralateral hemifield. Taken together, our results indicate an FEF involvement in evidence accumulation but not categorization, and suggest hemispheric lateralization for this function in the human brain.
Sensory perception relies on fitness-maximizing codes
Schaffner, Jonathan; Bao, Sherry Dongqi; Tobler, Philippe N.; et al. (2023)
Nature Human Behaviour
Sensory information encoded by humans and other organisms is generally presumed to be as accurate as their biological limitations allow. However, perhaps counterintuitively, accurate sensory representations may not necessarily maximize the organism's chances of survival. To test this hypothesis, we developed a unified normative framework for fitness-maximizing encoding by combining theoretical insights from neuroscience, computer science, and economics. Behavioural experiments in humans revealed that sensory encoding strategies are flexibly adapted to promote fitness maximization, a result confirmed by deep neural networks with information capacity constraints trained to solve the same task as humans. Moreover, human functional MRI data revealed that novel behavioural goals that rely on object perception induce efficient stimulus representations in early sensory structures. These results suggest that fitness-maximizing rules imposed by the environment are applied at early stages of sensory processing in humans and machines.
The parietal cortex has a causal role in ambiguity computations in humans
Valdebenito-Oyarzo, Gabriela; Paz Martínez-Molina, María; Soto-Icaza, Patricia; et al. (2024)
PLoS Biology
Humans often face the challenge of making decisions between ambiguous options. The level of ambiguity in decision-making has been linked to activity in the parietal cortex, but its exact computational role remains elusive. To test the hypothesis that the parietal cortex plays a causal role in computing ambiguous probabilities, we conducted consecutive fMRI and TMS-EEG studies. We found that participants assigned unknown probabilities to objective probabilities, elevating the uncertainty of their decisions. Parietal cortex activity correlated with the objective degree of ambiguity and with a process that underestimates the uncertainty during decision-making. Conversely, the midcingulate cortex (MCC) encodes prediction errors and increases its connectivity with the parietal cortex during outcome processing. Disruption of the parietal activity increased the uncertainty evaluation of the options, decreasing cingulate cortex oscillations during outcome evaluation and lateral frontal oscillations related to value ambiguous probability. These results provide evidence for a causal role of the parietal cortex in computing uncertainty during ambiguous decisions made by humans.
Rationality, preferences, and emotions with biological constraints: it all starts from our senses
Polania, Rafael Hernan; Burdakov, Denis; Hare, Todd A. (2024)
Trends in Cognitive Sciences
Is the role of our sensory systems to represent the physical world as accurately as possible? If so, are our preferences and emotions, often deemed irrational, decoupled from these 'ground-truth' sensory experiences? We show why the answer to both questions is 'no'. Brain function is metabolically costly, and the brain loses some fraction of the information that it encodes and transmits. Therefore, if brains maximize objective functions that increase the fitness of their species, they should adapt to the objective-maximizing rules of the environment at the earliest stages of sensory processing. Consequently, observed 'irrationalities', preferences, and emotions stem from the necessity for our early sensory systems to adapt and process information while considering the metabolic costs and internal states of the organism.
Lateral prefrontal theta oscillations causally drive a computational mechanism underlying conflict expectation and adaptation
Martínez-Molina, María Paz; Valdebenito-Oyarzo, Gabriela; Soto-Icaza, Patricia; et al. (2024)
Nature Communications
Adapting our behavior to environmental demands relies on our capacity to perceive and manage potential conflicts within our surroundings. While evidence implicates the involvement of the lateral prefrontal cortex and theta oscillations in detecting conflict stimuli, their causal role in conflict expectation remains elusive. Consequently, the exact computations and neural mechanisms underlying these cognitive processes still need to be determined. We employed an integrative approach involving cognitive computational modeling, fMRI, TMS, and EEG to establish a causal link between oscillatory brain function, its neurocomputational role, and the resulting conflict processing and adaptation behavior. Our results reveal a computational process underlying conflict expectation, which correlates with BOLD-fMRI and theta activity in the superior frontal gyrus (SFG). Modulation of theta activity via rhythmic TMS applied over the SFG induces endogenous theta activity, which in turn enhances computations associated with conflict expectation. These findings provide evidence for the causal involvement of SFG theta activity in learning and allocating cognitive resources to address forthcoming conflict stimuli.

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Rafael Hernan Polania

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