Neural plasticity in decision making and memory formation

Goal-directed behaviour is characterized by an ability to make inferences without direct experience. This requires a model of the environment and of ourselves, which is flexibly adjusted in light of new incoming information. This thesis uses representational functional magnetic resonance imaging (fMRI) techniques in combination with computational modelling to investigate (1) whether humans can construct models of other people’s preferences and whether this process influences their own value representation, and (2) how statistical relationships between discrete, non-spatial objects are combined into a model of the world. The first part of the thesis investigates how subjective values are computed in an intertemporal choice paradigm, and how these value computations are updated as a consequence of learning about the preferences of another. Critically, subjects’ own preferences shift towards those of the other when learning about their choices, suggesting that subjects incorporate new knowledge about others into a model of their own preferences. The underlying mechanism involves prediction errors, which introduce plasticity into subjects’ mPFC value representations, in turn resulting in a shift in subjects’ own preferences. The second part of this thesis investigates how relationships between arbitrary objects are represented in the brain. Relational knowledge is often considered analogous to spatial reasoning, where relationships are encoded in a hippocampal-entorhinal ‘cognitive map’. Here, I show that maps can also be extracted from the entorhinal cortex for discrete relationships between arbitrary stimuli, and in the absence of conscious knowledge. The representation of abstract knowledge in map-like structures suggests that inferences do not need to rely on direct experiences but can be computed anew from mapped knowledge. Together, these studies reveal how world models are represented and updated at the level of neural representations, providing a bridge between representational codes and cognitive computations

Reciprocity of Social Influence

Humans seek advice, via social interaction, to improve their decisions. While social interaction is often reciprocal, the role of reciprocity in social influence is unknown. Here, we tested the hypothesis that our influence on others affects how much we are influenced by them. Participants first made a visual perceptual estimate and then shared their estimate with an alleged partner. Then, in alternating trials, the participant either revised their decisions or observed how the partner revised theirs. We systematically manipulated the partner's susceptibility to influence from the participant. We show that participants reciprocated influence with their partner by gravitating toward the susceptible (but not insusceptible) partner's opinion. In further experiments, we showed that reciprocity is both a dynamic process and is abolished when people believed that they interacted with a computer. Reciprocal social influence is a signaling medium for human-to-human communication that goes beyond aggregation of evidence for decision improvement

Spike-Triggered Covariance Analysis Reveals Phenomenological Diversity of Contrast Adaptation in the Retina

When visual contrast changes, retinal ganglion cells adapt by adjusting their sensitivity as well as their temporal filtering characteristics. The latter has classically been described by contrast-induced gain changes that depend on temporal frequency. Here, we explored a new perspective on contrast-induced changes in temporal filtering by using spike-triggered covariance analysis to extract multiple parallel temporal filters for individual ganglion cells. Based on multielectrode-array recordings from ganglion cells in the isolated salamander retina, we found that contrast adaptation of temporal filtering can largely be captured by contrast-invariant sets of filters with contrast-dependent weights. Moreover, differences among the ganglion cells in the filter sets and their contrast-dependent contributions allowed us to phenomenologically distinguish three types of filter changes. The first type is characterized by newly emerging features at higher contrast, which can be reproduced by computational models that contain response-triggered gain-control mechanisms. The second type follows from stronger adaptation in the Off pathway as compared to the On pathway in On-Off-type ganglion cells. Finally, we found that, in a subset of neurons, contrast-induced filter changes are governed by particularly strong spike-timing dynamics, in particular by pronounced stimulus-dependent latency shifts that can be observed in these cells. Together, our results show that the contrast dependence of temporal filtering in retinal ganglion cells has a multifaceted phenomenology and that a multi-filter analysis can provide a useful basis for capturing the underlying signal-processing dynamics

Repetition suppression: a means to index neural representations using BOLD?

Understanding how the human brain gives rise to complex cognitive processes remains one of the biggest challenges of contemporary neuroscience. While invasive recording in animal models can provide insight into neural processes that are conserved across species, our understanding of cognition more broadly relies upon investigation of the human brain itself. There is therefore an imperative to establish non-invasive tools that allow human brain activity to be measured at high spatial and temporal resolution. In recent years, various attempts have been made to refine the coarse signal available in functional magnetic resonance imaging (fMRI), providing a means to investigate neural activity at the meso-scale, i.e. at the level of neural populations. The most widely used techniques include repetition suppression and multivariate pattern analysis. Human neuroscience can now use these techniques to investigate how representations are encoded across neural populations and transformed by relevant computations. Here, we review the physiological basis, applications and limitations of fMRI repetition suppression with a brief comparison to multivariate techniques. By doing so, we show how fMRI repetition suppression holds promise as a tool to reveal complex neural mechanisms that underlie human cognitive function.This article is part of the themed issue 'Interpreting BOLD: a dialogue between cognitive and cellular neuroscience'

Entorhinal and ventromedial prefrontal cortices abstract and generalize the structure of reinforcement learning problems.

Knowledge of the structure of a problem, such as relationships between stimuli, enables rapid learning and flexible inference. Humans and other animals can abstract this structural knowledge and generalize it to solve new problems. For example, in spatial reasoning, shortest-path inferences are immediate in new environments. Spatial structural transfer is mediated by cells in entorhinal and (in humans) medial prefrontal cortices, which maintain their co-activation structure across different environments and behavioral states. Here, using fMRI, we show that entorhinal and ventromedial prefrontal cortex (vmPFC) representations perform a much broader role in generalizing the structure of problems. We introduce a task-remapping paradigm, where subjects solve multiple reinforcement learning (RL) problems differing in structural or sensory properties. We show that, as with space, entorhinal representations are preserved across different RL problems only if task structure is preserved. In vmPFC and ventral striatum, representations of prediction error also depend on task structure

Learning-induced plasticity in medial prefrontal cortex predicts preference malleability

Learning induces plasticity in neuronal networks. As neuronal populations contribute to multiple representations, we reasoned plasticity in one representation might influence others. We used human fMRI repetition suppression to show that plasticity induced by learning another individual's values impacts upon a value representation for oneself in medial prefrontal cortex (mPFC), a plasticity also evident behaviorally in a preference shift. We show this plasticity is driven by a striatal "prediction error," signaling the discrepancy between the other's choice and a subject's own preferences. Thus, our data highlight that mPFC encodes agent-independent representations of subjective value, such that prediction errors simultaneously update multiple agents' value representations. As the resulting change in representational similarity predicts interindividual differences in the malleability of subjective preferences, our findings shed mechanistic light on complex human processes such as the powerful influence of social interaction on beliefs and preferences