Brains balance actions and responses

Traditionally, the neurosciences have been working under the assumption of the sensorimotor hypothesis, namely that the main function of brains is to compute motor output from sensory input. At the same time, ecologists have known for a long time that such passive strategies are not evolutionarily stable. Instead, animals must be constantly active, exploring, probing the environment with spontaneous actions and planning future actions by learning from behavioral consequences. Today, output-input as well as input-output computations are regarded as equally important mechanisms of action selection. This insight entails that general brain function can be best described as computing the balance between actions and responses, or, in ecological terms, balancing exploration and exploitation. From a neurophysiological perspective, brains balance exogenous with endogenous processing.

The human default mode network

This shift in perspective, from passively responding brains to spontaneously acting brains opened a new avenue in the neurosciences: how do brains generate spontaneous activity? In the last decade, functional magnetic resonance imaging (fMRI) in humans and non-human primates has provided insights on a phenomenon the dynamics of which provide a hypothetical mechanism by which this balance may be achieved. The so-called 'default-mode network' interacts in a push-pull fashion with task-related networks such that they mutually inhibit each other. Whenever no particular task is being solved by the person in the fMRI scanner, the default-mode network is active; whenever a task is being computed, a task-related network is active and the default-mode network is attenuated. Importantly, behavioral variability during a task can be explained to a large extent by the fluctuations in the activity of the attenuated default-mode network. Moreover, mistakes during a task are often preceded by activation of the default-mode network. Finally, many psychiatric disorders which affect action selection also affect the structure, connectivity and dynamics of the default-mode network.

Studying spontaneity in invertebrates

However, humans are a poor study subject for a functional analysis of neurobiological processes. Early experiments in invertebrates, notably insects, suggested that spontaneous activity was a property of all brains, opening up the possibility to use the genetic toolbox of the fruit fly Drosophila to study the neurobiology of spontaneous behavior. Indeed, these early ethological studies matched ecological research suggesting that spontaneous behavioral variability was an adaptive trait selected for by evolution due to several different functions:

• Render the animal unpredictable to prey, predators or competitors
• Discover hidden resources
• Identify the stimuli in the sensory stream which are controlled by the animal itself

In our quest for the neurobiological substrate of spontaneity, we started out with a mathematical analysis of spontaneous flight behavior, which set out to test if the variability observed in the fly turning behavior was due to random noise or initiated by decision-making circuits in the fly brain. After we found evidence for nonlinear decision-making circuits controlling Drosophila turning behavior, we have started a project localizing these circuits in the fly brain, using the genetic tools available for our model system.

It is inescapable to notice that the ability to initiate spontaneous behavior does have implications for the question of whether we have free will. Therefore, I have proposed a scientific framework for the term 'free will', based on the ability of all animals to spontaneously vary their behavior.