Sensory Processing in the Dorsolateral Striatum: The Contribution of Thalamostriatal Pathways

Abstract

The dorsal striatum has two functionally-defined subdivisions: a dorsomedial striatum (DMS) region involved in mediating goal-directed behaviors that require conscious effort, and a dorsolateral striatum (DLS) region involved in the execution of habitual behaviors in a familiar sensory context. Consistent with its presumed role in forming stimulus-response (S-R) associations, neurons in DLS receive massive inputs from sensorimotor cortex and are responsive to both active and passive sensory stimulation. While several studies have established that corticostriatal inputs contribute to the stimulus-induced responses observed in the DLS, there is growing awareness that the thalamus has a significant role in conveying sensory-related information to DLS and other parts of the striatum. The thalamostriatal projections to DLS originate mainly from the caudal intralaminar region, which contains the parafascicular (Pf) nucleus, and from higher-order thalamic nuclei such as the medial part of the posterior (POm) nucleus. Based on recent findings, we hypothesize that the thalamostriatal projections from these two regions exert opposing influences on the expression of behavioral habits. This article reviews the subcortical circuits that regulate the transmission of sensory information through these thalamostriatal projection systems, and describes the evidence that indicates these circuits could be manipulated to ameliorate the symptoms of Parkinson’s disease (PD) and related neurological disorders.

Cholinergic modulation of striatal microcircuits

“…Long‐term changes in striatal excitability by cortical and thalamic axonal stimulation could be related to their different proposed functions: goal‐directed behavior for cortical afferents (Graybiel, ) and attention and arousal for thalamic afferents (Alloway et al., ).…”

“…Long-term changes in striatal excitability by cortical and thalamic axonal stimulation could be related to their different proposed functions: goal-directed behavior for cortical afferents (Graybiel, 1995) and attention and arousal for thalamic afferents (Alloway et al, 2017). These selected references by no means reflect all the evidence gathered through more than 40 years of research, apologies for unintended omissions.…”

Cognitive capacity limits are remediated by practice-induced plasticity between the Putamen and Pre-Supplementary Motor Area

“…First we asked which region in the network received driving inputs that are modulated by multitasking demands. As the IPS shows sensitivity to sensory inputs across modalities (Vossel, Geng, and Fink 2014;Anderson et al 2010;Grefkes and Fink 2005) , and as the striatum receives sensory-inputs from both the thalamus (Alloway et al 2017) and from sensory cortices (Saint-Cyr, Ungerleider, and Desimone 1990; Guo et al 2018;Reig and Silberberg 2014) , both IPS and putamen were considered as possible candidates. We therefore fit each of the 63 modulatory models twice, once allowing driving inputs to occur via the IPS, and once allowing input via the putamen (therefore, total models [ M i ] = 126 ).…”

Translating striatal activity from brain slice to whole animal neurophysiology: A guide for neuroscience research integrating diverse levels of analysis

“…The predicted straightforward reduction in activity was not the primary outcome in several studies and this led to the formulation of the ideas that these striatal cells could actually be "released" in some forms after neocortical damage and possibly "driven" by other afferents besides the massive cortical input. For example, subregions such as the parafascicular and medial part of the posterior nuclei have been proposed to play distinct roles in mediating behavioral habit formation by regulating or "gating" sensory information flow in dorsolateral striatum (Alloway, Smith, Mowery, & Watson, 2017). Early work by Buchwald and colleagues supported a strong role for thalamic afferents arising to the striatum Cherubini et al, 1979).…”

“…Recent work has focused on this thalamostriatal pathway as another modulator of distinct cell types within the striatum. For example, subregions such as the parafascicular and medial part of the posterior nuclei have been proposed to play distinct roles in mediating behavioral habit formation by regulating or "gating" sensory information flow in dorsolateral striatum (Alloway, Smith, Mowery, & Watson, 2017).…”