Surprise
surprise
CNS Control of Peripheral Mitochondrial Form and Function: Mitokines
My laboratory has made an intriguing discovery that mitochondrial stress in one tissue can be communicated to distal tissues. We find that mitochondrial stress in the nervous system triggers the production of entities known as mitokines. These mitokines are discharged from the nervous system, orchestrating a response in peripheral tissues that extends the lifespan of C. elegans. The revelation came as a surprise, given the prevalent belief that cell autonomous mechanisms would underlie the relationship between mitochondrial function and aging. It was also surprising given the prevailing dogma that mitochondrial function must be increased, not decreased, to improve health and longevity. Our work also underscores the fact that mitochondria, which originated as a microbial entity and later evolved into an intracellular symbiont, have retained their capacity for intercommunication, now facilitated by signals from the nervous system. We hypothesize that this communication has evolved as a mechanism to reduce infection from pathogens.
Piecing together the puzzle of emotional consciousness
Conscious emotional experiences are very rich in their nature, and can encompass anything ranging from the most intense panic when facing immediate threat, to the overwhelming love felt when meeting your newborn. It is then no surprise that capturing all aspects of emotional consciousness, such as intensity, valence, and bodily responses, into one theory has become the topic of much debate. Key questions in the field concern how we can actually measure emotions and which type of experiments can help us distill the neural correlates of emotional consciousness. In this talk I will give a brief overview of theories of emotional consciousness and where they disagree, after which I will dive into the evidence proposed to support these theories. Along the way I will discuss to what extent studying emotional consciousness is ‘special’ and will suggest several tools and experimental contrasts we have at our disposal to further our understanding on this intriguing topic.
Three-factor rules of synaptic plasticity: from reward to surprise
Off-policy learning in the basal ganglia
I will discuss work with Jack Lindsey modeling reinforcement learning for action selection in the basal ganglia. I will argue that the presence of multiple brain regions, in addition to the basal ganglia, that contribute to motor control motivates the need for an off-policy basal ganglia learning algorithm. I will then describe a biological implementation of such an algorithm that predicts tuning of dopamine neurons to a quantity we call "action surprise," in addition to reward prediction error. In the same model, an implementation of learning from a motor efference copy also predicts a novel solution to the problem of multiplexing feedforward and efference-related striatal activity. The solution exploits the difference between D1 and D2-expressing medium spiny neurons and leads to predictions about striatal dynamics.
Naturalistic violation of expectations reveal hierarchical surprise responses in the human brain
An economic decision-making model of anticipated surprise with dynamic expectation
When making decision under risk, people often exhibit behaviours that classical economic theories cannot explain. Newer models that attempt to account for these ‘irrational’ behaviours often lack neuroscience bases and require the introduction of subjective and problem-specific constructs. Here, we present a decision-making model inspired by the prediction error signals and introspective neuronal replay reported in the brain. In the model, decisions are chosen based on ‘anticipated surprise’, defined by a nonlinear average of the differences between individual outcomes and a reference point. The reference point is determined by the expected value of the possible outcomes, which can dynamically change during the mental simulation of decision-making problems involving sequential stages. Our model elucidates the contribution of each stage to the appeal of available options in a decision-making problem. This allows us to explain several economic paradoxes and gambling behaviours. Our work could help bridge the gap between decision-making theories in economics and neurosciences.
Through the bottleneck: my adventures with the 'Tishby program'
One of Tali's cherished goals was to transform biology into physics. In his view, biologists were far too enamored by the details of the specific models they studied, losing sight of the big principles that may govern the behavior of these models. One such big principle that he suggested was the 'information bottleneck (IB) principle'. The iIB principle is an information-theoretical approach for extracting the relevant information that one random variable carries about another. Tali applied the IB principle to numerous problems in biology, gaining important insights in the process. Here I will describe two applications of the IB principle to neurobiological data. The first is the formalization of the notion of surprise that allowed us to rigorously estimate the memory duration and content of neuronal responses in auditory cortex, and the second is an application to behavior, allowing us to estimate 'optimal policies under information constraints' that shed interesting light on rat behavior.
Active sleep in flies: the dawn of consciousness
The brain is a prediction machine. Yet the world is never entirely predictable, for any animal. Unexpected events are surprising and this typically evokes prediction error signatures in animal brains. In humans such mismatched expectations are often associated with an emotional response as well. Appropriate emotional responses are understood to be important for memory consolidation, suggesting that valence cues more generally constitute an ancient mechanism designed to potently refine and generalize internal models of the world and thereby minimize prediction errors. On the other hand, abolishing error detection and surprise entirely is probably also maladaptive, as this might undermine the very mechanism that brains use to become better prediction machines. This paradoxical view of brain functions as an ongoing tug-of-war between prediction and surprise suggests a compelling new way to study and understand the evolution of consciousness in animals. I will present approaches to studying attention and prediction in the tiny brain of the fruit fly, Drosophila melanogaster. I will discuss how an ‘active’ sleep stage (termed rapid eye movement – REM – sleep in mammals) may have evolved in the first animal brains as a mechanism for optimizing prediction in motile creatures confronted with constantly changing environments. A role for REM sleep in emotional regulation could thus be better understood as an ancient sleep function that evolved alongside selective attention to maintain an adaptive balance between prediction and surprise. This view of active sleep has some interesting implications for the evolution of subjective awareness and consciousness.
The evolutionary and psychological origins of reciprocal cooperation
If only those behaviours evolve that increase the actor’s own survival and reproductive success, then it might come as a surprise that cooperative behaviours, i.e. providing benefits to others, are a widespread phenomenon. Many animals cooperate even with unrelated individuals in various contexts, like providing care or food. One possibility to explain these behaviours is reciprocity. Reciprocal cooperation, i.e. helping those that were helpful before, is a ubiquitous and important trait of human sociality. Still, the evolutionary origin of it is largely unclear, mainly because it is believed that other animals do not exchange help reciprocally. Consequently, reciprocity is suggested to have evolved in the human lineage only. In contrast to this, I propose that reciprocity is not necessarily cognitively demanding and likely to be widespread. In my talk, I will first shed light on the mechanisms of reciprocal cooperation in Norway rats (Rattus norvegicus). In a series of studies, my colleagues and I have demonstrated that Norway rats reciprocally exchange goods and services between and within different commodities and independent of kinship. Furthermore, to understand the evolutionary origins of human reciprocity, and whether it is shared with other animals, I will then discuss evidence for reciprocity in non-human primates, which are our closest living relatives. A thorough analysis of the findings showed that reciprocity is present and, for example, not confined to unrelated individuals, but that the choice of commodities can impact the likelihood of reciprocation. Based on my findings, I conclude that reciprocal cooperation in non-human animals is present but largely neglected and not restricted to humans. In order to deepen our understanding of the evolutionary origins of reciprocity in more general, future studies should investigate when and how reciprocity in non-human animals emerged and how it is maintained.
Surprises in self-deforming self-propelling systems
From slithering snakes, to entangling robots, self-deforming (shape changing) active systems display surprising dynamics. This is particularly true when such systems interact with environments or other agents to generate self-propulsion (movement). In this talk, I will discuss a few projects from my group illustrating unexpected effects in individual and collectives of self-deformers. For example, snakes and snake-like robots mechanically “diffract” from fixed environmental heterogeneities, collections of smart-active robots (smarticles) can locomote (and phototax) as a collective despite individual immobility, and geometrically actively entangling ensembles of blackworms and robots can self-propel as a unit to thermo or phototax without centralized control.
Neural sequence representation of stimulus value, response and surprise in hippocampus and prefrontal cortex
COSYNE 2022
Neural sequence representation of stimulus value, response and surprise in hippocampus and prefrontal cortex
COSYNE 2022
Theories of surprise: definitions and predictions
COSYNE 2022
Theories of surprise: definitions and predictions
COSYNE 2022
Neural encoding of sensory “surprise” in the mouse cortex
FENS Forum 2024
Sensory surprise signals in the visual cortex of the anesthetized mouse
FENS Forum 2024