Humans and other animals approach reward and avoid punishment and pay attention to cues predicting these events. Such motivated behavior thus appears to be guided by value, which directs behavior towards or away from positively or negatively valenced outcomes. Moreover, it is facilitated by (top-down) salience, which enhances attention to behaviorally relevant learned cues predicting the occurrence of valenced outcomes. Using human neuroimaging, we recently separated value (ventral striatum, posterior ventromedial prefrontal cortex) from salience (anterior ventromedial cortex, occipital cortex) in the domain of liquid reward and punishment. Moreover, we investigated potential drivers of learned salience: the probability and uncertainty with which valenced and non-valenced outcomes occur. We find that the brain dissociates valenced from non-valenced probability and uncertainty, which indicates that reinforcement matters for the brain, in addition to information provided by probability and uncertainty alone, regardless of valence. Finally, we assessed learning signals (unsigned prediction errors) that may underpin the acquisition of salience. Particularly the insula appears to be central for this function, encoding a subjective salience prediction error, similarly at the time of positively and negatively valenced outcomes. However, it appears to employ domain-specific time constants, leading to stronger salience signals in the aversive than the appetitive domain at the time of cues. These findings explain why previous research associated the insula with both valence-independent salience processing and with preferential encoding of the aversive domain. More generally, the distinction of value and salience appears to provide a useful framework for capturing the neural basis of motivated behavior.

Neural representations of time are central to our understanding of the world around us. I review cognitive, neurophysiological and theoretical work that converges on three simple ideas. First, the time of past events is remembered via populations of neurons with a continuum of functional time constants. Second, these time constants evenly tile the log time axis. This results in a neural Weber-Fechner scale for time which can support behavioral Weber-Fechner laws and characteristic behavioral effects in memory experiments. Third, these populations appear as dual pairs---one type of population contains cells that change firing rate monotonically over time and a second type of population that has circumscribed temporal receptive fields. These ideas can be used to build artificial neural networks that have novel properties. Of particular interest, a convolutional neural network built using these principles can generalize to arbitrary rescaling of its inputs. That is, after learning to perform a classification task on a time series presented at one speed, it successfully classifies stimuli presented slowed down or sped up. This result illustrates the point that this confluence of ideas originating in cognitive psychology and measured in the mammalian brain could have wide-reaching impacts on AI research.

Low-dimensional population dynamics can be observed in neural activity recorded from the prefrontal cortex (PFC) of subjects performing simple cognitive tasks. Many studies have shown that recurrent neural networks (RNNs) trained on the same tasks can reproduce qualitatively these state space trajectories, and have used them as models of how neuronal dynamics implement task computations. The PFC is also viewed as a conductor that organizes the communication between cortical areas and provides contextual information. It is then not clear what is its role in solving simple cognitive tasks. Do the low-dimensional trajectories observed in the PFC really correspond to the computations that it performs? Or do they indirectly reflect the computations occurring within the cortical areas projecting to the PFC? To address these questions, we modelled cortical areas with a modular RNN and equipped it with a PFC-like cognitive system. When trained on cognitive tasks, this multi-system brain model can reproduce the low-dimensional population responses observed in neuronal activity as well as classical RNNs. Qualitatively different mechanisms can emerge from the training process when varying some details of the architecture such as the time constants. In particular, there is one class of models where it is the dynamics of the cognitive system that is implementing the task computations, and another where the cognitive system is only necessary to provide contextual information about the task rule as task performance is not impaired when preventing the system from accessing the task inputs. These constitute two different hypotheses about the causal role of the PFC in solving simple cognitive tasks, which could motivate further experiments on the brain.

Modular structures in myriad forms — genetic, structural, functional — are ubiquitous in the brain. While modularization may be shaped by genetic instruction or extensive learning, the mechanisms of module emergence are poorly understood. Here, we explore complementary mechanisms in the form of bottom-up dynamics that push systems spontaneously toward modularization. As a paradigmatic example of modularity in the brain, we focus on the grid cell system. Grid cells of the mammalian medial entorhinal cortex (mEC) exhibit periodic lattice-like tuning curves in their encoding of space as animals navigate the world. Nearby grid cells have identical lattice periods, but at larger separations along the long axis of mEC the period jumps in discrete steps so that the full set of periods cluster into 5-7 discrete modules. These modules endow the grid code with many striking properties such as an exponential capacity to represent space and unprecedented robustness to noise. However, the formation of discrete modules is puzzling given that biophysical properties of mEC stellate cells (including inhibitory inputs from PV interneurons, time constants of EPSPs, intrinsic resonance frequency and differences in gene expression) vary smoothly in continuous topographic gradients along the mEC. How does discreteness in grid modules arise from continuous gradients? We propose a novel mechanism involving two simple types of lateral interaction that leads a continuous network to robustly decompose into discrete functional modules. We show analytically that this mechanism is a generic multi-scale linear instability that converts smooth gradients into discrete modules via a topological “peak selection” process. Further, this model generates detailed predictions about the sequence of adjacent period ratios, and explains existing grid cell data better than existing models. Thus, we contribute a robust new principle for bottom-up module formation in biology, and show that it might be leveraged by grid cells in the brain.

The brain has a hugely diverse, heterogeneous structure. By contrast, many functional neural models are homogeneous. We compared the performance of spiking neural networks trained to carry out difficult tasks, with varying degrees of heterogeneity. Introducing heterogeneity in membrane and synapse time constants substantially improved task performance, and made learning more stable and robust across multiple training methods, particularly for tasks with a rich temporal structure. In addition, the distribution of time constants in the trained networks closely matches those observed experimentally. We suggest that the heterogeneity observed in the brain may be more than just the byproduct of noisy processes, but rather may serve an active and important role in allowing animals to learn in changing environments.

Engineered pattern-recognition systems strive for short time-to-solution and low energy-to-solution characteristics. This represents one of the main driving forces behind the development of neuromorphic devices. For both them and their biological archetypes, this corresponds to using as few spikes as early as possible. The concept of few and early spikes is used as the founding principle in the time-to-first-spike coding scheme. Within this framework, we have developed a spike-timing-based learning algorithm, which we used to train neuronal networks on the mixed-signal neuromorphic platform BrainScaleS-2. We derive, from first principles, error-backpropagation-based learning in networks of leaky integrate-and-fire (LIF) neurons relying only on spike times, for specific configurations of neuronal and synaptic time constants. We explicitly examine applicability to neuromorphic substrates by studying the effects of reduced weight precision and range, as well as of parameter noise. We demonstrate the feasibility of our approach on continuous and discrete data spaces, both in software simulations and on BrainScaleS-2. This narrows the gap between previous models of first-spike-time learning and biological neuronal dynamics and paves the way for fast and energy-efficient neuromorphic applications.