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Midline Thalamic Damage Associated with Alcohol-Use Disorders: Disruption of Distinct Thalamocortical Pathways and Function

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Abstract

The thalamus, a significant part of the diencephalon, is a symmetrical and bilateral central brain structure. The thalamus is subdivided into three major groups of nuclei based on their function: sensorimotor nuclei (or principal/relay nuclei), limbic nuclei and nuclei bridging these two domains. Anatomically, nuclei within the thalamus are described by their location, such as anterior, medial, lateral, ventral, and posterior. In this review, we summarize the role of medial and midline thalamus in cognition, ranging from learning and memory to flexible adaptation. We focus on the discoveries in animal models of alcohol-related brain damage, which identify the loss of neurons in the medial and midline thalamus as drivers of cognitive dysfunction associated with alcohol use disorders. Models of developmental ethanol exposure and models of adult alcohol-related brain damage and are compared and contrasted, and it was revealed that there are similar (anterior thalamus) and different (intralaminar [adult exposure] versus ventral midline [developmental exposure]) thalamic pathology, as well as disruptions of thalamo-hippocampal and thalamo-cortical circuits. The final part of the review summarizes approaches to recover alcohol-related brain damage and cognitive and behavioral outcomes. These approaches include pharmacological, nutritional and behavioral interventions that demonstrated the potential to mitigate alcohol-related damage. In summary, the medial/midline thalamus is a significant contributor to cognition function, which is also sensitive to alcohol-related brain damage across the life span, and plays a role in alcohol-related cognitive dysfunction.

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Abbreviations

AC:

Anterior cingulate cortex

ACh:

Acetylcholine

AD:

Anterodorsal thalamic nucleus

AM:

Anteromedial thalamic nucleus

ATN:

Anterior thalamic nucleus

AV:

Anteroventral thalamic nucleus

AVVL:

Anteroventral ventrolateral nucleus

BAC:

Blood alcohol concentration

BDNF:

Brain derived neurotrophin factor

CE:

Complex environment

CET:

Chronic ethanol treatment

CL:

Central lateral thalamic nucleus

CM:

Central medial thalamic nucleus

DREADDs:

Designer Receptors Exclusively Activated by Designer Drugs

E:

Embryonic day

EAS:

Early acute stage

EC:

Entorhinal cortex

EE:

Enriched environment

FAS:

Fetal Alcohol Syndrome

FASD:

Fetal Alcohol Spectrum Disorders

HD:

Head direction

IAM:

Interoanteromedial thalamic nucleus

IkBa:

Nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor, alpha

IL:

Infralimbic cortex

IL-1β:

Interleukin-1β

IL-6:

Interleukin-6

IMD:

Intermediodorsal thalamic nuclei

KS:

Korsakoff Syndrome

LAS:

Late acute stage

MAS:

Middle acute stage

MO:

Medial orbital cortex

mPFC:

Medial prefrontal cortex

MRI:

Magnetic resonance imaging

MS/dB:

Medial septum/diagonal band

NGF:

Nerve growth factor

NMTP:

Non-matching-to-position

PC:

Paracentral thalamic nucleus

PD:

Postnatal day

PF:

Parafascicular thalamic nucleus

PL:

Prelimbic cortex

PTD:

Pyrithiamine-induced thiamine deficiency

Re:

Nucleus reuniens

Rh:

Rhomboid nucleus

SPF:

Subparafascicular thalamic nucleus

TNF-ɑ:

Tumor necrosis factor-ɑ

VEGF:

Vascular endothelial growth factor

WE:

Wernicke’s Encephalopathy

WKS:

Wernicke-Korsakoff Syndrome

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Acknowledgements

Supported by NIH grant numbers R21AA026613 and R01AA027269 to A.Y.K., and P50AA017823-Main 2 and R01AA021775 to L.M.S. and the Developmental Exposure Alcohol Research Center at Binghamton University.

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  1. Developmental Ethanol Alcohol Research Center, Department of Psychology, Binghamton University, State University of New York, Binghamton, NY, 13902-6000, USA

    Lisa M. Savage & Polliana T. Nunes

  2. Department of Psychological and Brain Sciences, University of Delaware, Newark, DE, USA

    Zachary H. Gursky, Katrina A. Milbocker & Anna Y. Klintsova

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Savage, L.M., Nunes, P.T., Gursky, Z.H. et al. Midline Thalamic Damage Associated with Alcohol-Use Disorders: Disruption of Distinct Thalamocortical Pathways and Function. Neuropsychol Rev 31, 447–471 (2021). https://doi.org/10.1007/s11065-020-09450-8

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