Revisiting the purpose of the thalamus: anatomically sub-cortical but functionally supra-cortical?

The largely accepted view of the brain function is corticocentric: the cerebral cortex monitors the world to provide optimal behavioural decisions given current external and internal demands. However, this overlooks a crucial fact: the cerebral cortex has very little direct input from the outside world, and hence is not in a position to monitor it. In fact, the cortex receives the majority of its information from the thalamus. As such, the cortex monitors the thalamus, while the thalamus monitors the external environment. Interactions between the two are controlled by inhibition from the thalamic reticular nucleus (TRN), which dynamically modifies the information transmitted by the thalamus to the cortex and vice versa. The thalamus is an evolutionarily conserved structure, present in all vertebrates. While it is increasingly clear that the thalamus is not a simple sensory relay, the exact purpose of this structure and of the thalamocortical architecture which separates the computational power of the cerebral cortex from direct access to information about the external world is not clear. Theoretical considerations regarding self-monitoring of brain function and observations of the behavioural impact of resective surgery elevate the thalamus in control terms from anatomically sub-cortical to functionally supra-cortical. They suggest that the final output of the system is determined, dynamically, at the thalamic level, driven by the integration of the cortical and sensory inputs with the current thalamic state. Investigating this idea to understand the role of the thalamus will require a concerted effort across electrophysiology, neuroimaging and computational approaches. • Thalamocortical architecture is conserved across vertebrates • Corticothalamic outnumber thalamocortical projections by an order of magnitude • The thalamocortical system may allow dynamic optimisation of performance • Thalamus integrates cortical and sensory inputs with the current thalamic state • Behavioural output is determined dynamically by the thalamus