The contribution of brain sub-cortical loops in the expression and acquisition of action understanding abilities

Abstract

Research on action understanding in cognitive neuroscience has led to the identification of a wide "action understanding network" mainly encompassing parietal and premotor cortical areas. Within this cortical network mirror neurons are critically involved implementing a neural mechanism according to which, during action understanding, observed actions are reflected in the motor patterns for the same actions of the observer. We suggest that focusing only on cortical areas and processes could be too restrictive to explain important facets of action understanding regarding, for example, the influence of the observer's motor experience, the multiple levels at which an observed action can be understood, and the acquisition of action understanding ability. In this respect, we propose that aside from the cortical action understanding network, sub-cortical processes pivoting on cerebellar and basal ganglia cortical loops could crucially support both the expression and the acquisition of action understanding abilities. Within the paper we will discuss how this extended view can overcome some limitations of the "pure" cortical perspective, supporting new theoretical predictions on the brain mechanisms underlying action understanding that could be tested by future empirical investigations.

Keywords: Action understanding; Basal ganglia cortical loops; Cerebellar cortical loops; Forward models; Inverse models; Mirror neurons; Neuroscience; Psychology; Sub-cortical processes.

Fig. 1

(a) Internal models within the mirror circuit. During action observation the circuit linking STS to F5 (STS-PFG-F5, solid arrows) may work as an inverse model, whereas during action execution the converse route from F5 to STS (F5-PFG-STS, dashed arrows) may act as a forward model (Miall, 2003). The inverse (b) and forward (c) models circuits within the mirror circuit and involving the cerebellum (CB). (d) Selection network within the mirror circuit involving basal ganglia (BG) and prefrontal cortex (PFC). The basal ganglia–cortical loops underlies actions competition within the mirror circuit (small-head arrows) whereas the PFC supplies the bias signal to select actions (large-head arrows). The basal ganglia also communicates with cerebellum through a bidirectional channel (dashed arrows).

Fig. 2

Sketch of the cerebellar cortical loops. The figure does not aim to supply a detailed overview of all the cerebellar components; rather, it focuses on the main interactions between the dentate output nuclei of the cerebellum and the target regions of the fronto-parietal cortex. PN: pontine nuclei; Cort: cerebellar cortex; vD: ventral dentate nucleus of the cerebellum; dD: dorsal dentate nucleus of the cerebellum; dlPFC: dorsal lateral areas of the PFC; PP: posterior parietal areas; PMC: premotor cortex; M1: primary motor areas; Ctx: cortex.

Fig. 3

Sketch of the three main cortico-striatal regions and their interconnections. Standard arrows indicate excitatory glutamate connections. Flat arrowheads indicate inhibitory GABA connections. Dot arrowheads indicate dopaminergic connections whereas dashed arrows indicate cross-loop connections. Reprinted with permission from Mcmillan Publishers Ltd: Nature Reviews Neuroscience, Yin and Knowlton (2006), copyright 2006.

Fig. 4

Schema of the neural circuits proposed to be mainly involved in action understanding processes. The dashed black arrow indicate the hyper direct pathway linking the subthalamic nucleus (STN) with the cortex (Ctx). The dashed gray arrows indicate the circuits interconnecting basal ganglia and cerebellum: an output stage of cerebellar processing, the dentate nucleus (DN), has a disynaptic connection with an input stage of basal ganglia processing, the striatum (Str) (Hoshi et al., 2005); there is also a reciprocal connection from the STN to the input stage of cerebellar processing, via pontine nuclei (PN), the cerebellar cortex (Cort) (Bostan et al., 2010, 2013). These interconnections enable two-way communication between the basal ganglia and cerebellum. Each of these subcortical modules receives signals from several areas of cerebral cortex through separate parallel channels (parallel solid black arrows) and sends signals (through Thalamus) to the cerebral cortex. The gray arrows and the black lines ending with a filled circle represent excitatory glutamatergic and inhibitory GABAergic projections, respectively. GPi, internal segment of the globus pallidus; GPe, external segment of the globus pallidus; SNr, substantia nigra pars reticulata. Some aspects of the schema arrangement are based on the proposals and results presented in Nambu et al. (2002), Hoshi et al. (2005), Bostan et al. (2010, 2013), and Baldassarre et al. (in press).