The intralaminar thalamus-an expressway linking visual stimuli to circuits determining agency and action selection

Abstract

Anatomical investigations have revealed connections between the intralaminar thalamic nuclei and areas such as the superior colliculus (SC) that receive short latency input from visual and auditory primary sensory areas. The intralaminar nuclei in turn project to the major input nucleus of the basal ganglia, the striatum, providing this nucleus with a source of subcortical excitatory input. Together with a converging input from the cerebral cortex, and a neuromodulatory dopaminergic input from the midbrain, the components previously found necessary for reinforcement learning in the basal ganglia are present. With this intralaminar sensory input, the basal ganglia are thought to play a primary role in determining what aspect of an organism's own behavior has caused salient environmental changes. Additionally, subcortical loops through thalamic and basal ganglia nuclei are proposed to play a critical role in action selection. In this mini review we will consider the anatomical and physiological evidence underlying the existence of these circuits. We will propose how the circuits interact to modulate basal ganglia output and solve common behavioral learning problems of agency determination and action selection.

Keywords: action selection; agency; basal ganglia; intralaminar; learning; plasticity; sensory.

Figure 1

Circuit diagrams illustrating (A) the synaptic relationships between key subcortical nuclei, and (B) the convergence in the striatum of learning signals from these nuclei. In both diagrams excitatory projections are green, inhibitory are red, and the neuromodulatory dopaminergic projection is in gray. (A) Putative subcortical loops are formed between the SC, rostral or caudal intralaminar nuclei, and through the basal ganglia to return to the SC. SNc, substantia nigra pars compacta; SNr/GPi, substantia nigra pars reticulata and globus pallidus internal segment. (B) Convergence onto striatal spiny projection neurons (labeled “S”) of a short-latency sensory signal from the SC, and a related short-latency dopaminergic signal from the SNc. When this conjunction is aligned with cortical input to spiny neurons, representing motor efferent copy, then the factors previously identified as necessary for potentiation of corticostriatal synapses are present (Reynolds and Wickens, 2002). CM/Pf, center median and parafascicular nuclei.

Figure 2

A potential model for competition between cortical and subcortical processing, via loops through the basal ganglia. Sensory input can be processed through different channels, with varying degrees of complexity in the processing operations. Subcortical processing through the basal ganglia, using relatively primitive sensorimotor systems, is adept at providing short-latency responses to salient stimuli (Schulz et al., 2009). Cortical processing through the basal ganglia is adept at longer-latency, more complex responses to stimuli. Cortical and subcortical requests for motor control can compete within the basal ganglia, with a “winner takes all” strategy necessary for effective behavioral selection (McHaffie et al., ; Redgrave et al., 2011). Diagram adapted with permission from P. Redgrave.