Thalamostriatal System Controls the Acquisition, Performance, and Flexibility of Learning Behavior

The dorsal striatum (DS) is a key structure of the basal ganglia circuitry, which regulates various types of learning processes and flexible switching of behavior. Intralaminar thalamic nuclei (ILNs) provide the main source of thalamostriatal inputs to the DS and constitute multiple nuclear groups, each of which innervates specific subdivisions of the striatum. Although the anatomical and electrophysiological properties of thalamostriatal neurons have been previously characterized, the behavioral and physiological functions of these neurons remain unclarified. Two representative thalamostriatal cell groups in the parafascicular nucleus (PF) and the central lateral nucleus (CL) are located in the caudal and rostral regions of the ILNs in rodents. Recently, the behavioral roles of these thalamostriatal cell groups have been investigated by the use of genetic and pharmacological manipulation techniques. In the current review, we summarize behavioral studies on thalamostriatal neurons, showing the key roles of these neurons in different learning processes, such as the acquisition, performance, and flexibility of behavior.

Rostral Intralaminar Thalamus Engagement in Cognition and Behavior

The thalamic rostral intralaminar nuclei (rILN) are a contiguous band of neurons that include the central medial, paracentral, and central lateral nuclei. The rILN differ from both thalamic relay nuclei, such as the lateral geniculate nucleus, and caudal intralaminar nuclei, such as the parafascicular nucleus, in afferent and efferent connectivity as well as physiological and synaptic properties. rILN activity is associated with a range of neural functions and behaviors, including arousal, pain, executive function, and action control. Here, we review this evidence supporting a role for the rILN in integrating arousal, executive and motor feedback information. In light of rILN projections out to the striatum, amygdala, and sensory as well as executive cortices, we propose that such a function enables the rILN to modulate cognitive and motor resources to meet task-dependent behavioral engagement demands.

Parafascicular Thalamic and Orbitofrontal Cortical Inputs to Striatum Represent States for Goal-Directed Action Selection

Several lines of evidence accrued over the last 5–10 years have converged to suggest that the parafascicular nucleus of the thalamus and the lateral orbitofrontal cortex each represent or contribute to internal state/context representations that guide action selection in partially observable task situations. In rodents, inactivations of each structure have been found to selectively impair performance in paradigms testing goal-directed action selection, but only when that action selection relies on state representations. Electrophysiological evidence has suggested that each structure achieves this function via inputs onto cholinergic interneurons (CINs) in the dorsomedial striatum. Here, we briefly review these studies, then point to anatomical evidence regarding the afferents of each structure and what they suggest about the specific features that each contribute to internal state representations. Finally, we speculate as to whether this role might be achieved interdependently through direct PF→OFC projections, or through the convergence of independent direct orbitofrontal cortex (OFC) and parafascicular nucleus of the thalamus (PF) inputs onto striatal targets.

Bidirectional control of fear memories by the cerebellum through the ventrolateral periaqueductal grey

Fear conditioning is a form of associative learning that is known to involve brain areas, notably the amygdala, the prefrontal cortex and the periaqueductal grey (PAG). Here, we describe the functional role of pathways that link the cerebellum with the fear network. We found that the cerebellar fastigial nucleus (FN) sends glutamatergic projections to vlPAG that synapse onto glutamatergic and GABAergic vlPAG neurons. Chemogenetic and optogenetic manipulations revealed that the FN-vlPAG pathway controls bi-directionally the strength of the fear memory, indicating a role in the association of the conditioned and unconditioned stimuli, a function consistent with vlPAG encoding of fear prediction error. In addition, we found that a FN - thalamic parafascicular nucleus pathway, which may relay cerebellar influence to the amygdala, is involved in anxiety and fear expression but not in fear memory. Our results reveal the contributions to the emotional system of the cerebellum, which exerts a potent control on the strength of the fear memory through excitatory FN-vlPAG projections.