Cerebellar state estimation enables resilient coupling across behavioural domains.

Cerebellar computations are necessary for fine behavioural control and may rely on internal models for estimation of behaviourally relevant states. Here, we propose that the central cerebellar function is to estimate how states interact with each other, and to use these estimates to coordinates extra-cerebellar neuronal dynamics underpinning a range of interconnected behaviours. To support this claim, we describe a cerebellar model for state estimation that includes state interactions, and link this model with the neuronal architecture and dynamics observed empirically. This is formalised using the free energy principle, which provides a dual perspective on a system in terms of both the dynamics of its physical-in this case neuronal-states, and the inferential process they entail. As a demonstration of this proposal, we simulate cerebellar-dependent synchronisation of whisking and respiration, which are known to be tightly coupled in rodents, as well as limb and tail coordination during locomotion. In summary, we propose that the ubiquitous involvement of the cerebellum in behaviour arises from its central role in precisely coupling behavioural domains.

Accounting for uncertainty: inhibition for neural inference in the cerebellum.

Sensorimotor coordination is thought to rely on cerebellar-based internal models for state estimation, but the underlying neural mechanisms and specific contribution of the cerebellar components is unknown. A central aspect of any inferential process is the representation of uncertainty or conversely precision characterizing the ensuing estimates. Here, we discuss the possible contribution of inhibition to the encoding of precision of neural representations in the granular layer of the cerebellar cortex. Within this layer, Golgi cells influence excitatory granule cells, and their action is critical in shaping information transmission downstream to Purkinje cells. In this review, we equate the ensuing excitation-inhibition balance in the granular layer with the outcome of a precision-weighted inferential process, and highlight the physiological characteristics of Golgi cell inhibition that are consistent with such computations.

On Markov blankets and hierarchical self-organisation.

Biological self-organisation can be regarded as a process of spontaneous pattern formation; namely, the emergence of structures that distinguish themselves from their environment. This process can occur at nested spatial scales: from the microscopic (e.g., the emergence of cells) to the macroscopic (e.g. the emergence of organisms). In this paper, we pursue the idea that Markov blankets - that separate the internal states of a structure from external states - can self-assemble at successively higher levels of organisation. Using simulations, based on the principle of variational free energy minimisation, we show that hierarchical self-organisation emerges when the microscopic elements of an ensemble have prior (e.g., genetic) beliefs that they participate in a macroscopic Markov blanket: i.e., they can only influence - or be influenced by - a subset of other elements. Furthermore, the emergent structures look very much like those found in nature (e.g., cells or organelles), when influences are mediated by short range signalling. These simulations are offered as a proof of concept that hierarchical self-organisation of Markov blankets (into Markov blankets) can explain the self-evidencing, autopoietic behaviour of biological systems.

The emergence of synchrony in networks of mutually inferring neurons.

This paper considers the emergence of a generalised synchrony in ensembles of coupled self-organising systems, such as neurons. We start from the premise that any self-organising system complies with the free energy principle, in virtue of placing an upper bound on its entropy. Crucially, the free energy principle allows one to interpret biological systems as inferring the state of their environment or external milieu. An emergent property of this inference is synchronisation among an ensemble of systems that infer each other. Here, we investigate the implications of neuronal dynamics by simulating neuronal networks, where each neuron minimises its free energy. We cast the ensuing ensemble dynamics in terms of inference and show that cardinal behaviours of neuronal networks - both in vivo and in vitro - can be explained by this framework. In particular, we test the hypotheses that (i) generalised synchrony is an emergent property of free energy minimisation; thereby explaining synchronisation in the resting brain: (ii) desynchronisation is induced by exogenous input; thereby explaining event-related desynchronisation and (iii) structure learning emerges in response to causal structure in exogenous input; thereby explaining functional segregation in real neuronal systems.