The primate basal ganglia: Parallel and integrative networks

Haber, Suzanne N.

doi:10.1016/j.jchemneu.2003.10.003

Cited by 1,479Neural and Behavioral Psychology StudiesNeurological disorders and treatmentsNeurotransmitter Receptor Influence on Behavior

The primate basal ganglia: Parallel and integrative networks

Haber, Suzanne N.·2003·Journal of Chemical Neuroanatomy

DOI 10.1016/j.jchemneu.2003.10.003

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Abstract

The basal ganglia and frontal cortex operate together to execute goal directed behaviors. This requires not only the execution of motor plans, but also the behaviors that lead to this execution, including emotions and motivation that drive behaviors, cognition that organizes and plans the general strategy, motor planning, and finally, the execution of that plan. The components of the frontal cortex that mediate these behaviors, are reflected in the organization, physiology, and connections between areas of frontal cortex and in their projections through basal ganglia circuits. This comprises a series of parallel pathways. However, this model does not address how information flows between circuits thereby developing new learned behaviors (or actions) from a combination of inputs from emotional, cognitive, and motor cortical areas. Recent anatomical evidence from primates demonstrates that the neuro-networks within basal ganglia pathways are in a position to move information across functional circuits. Two networks are: the striato-nigral-striatal network and the thalamo-cortical-thalamic network. Within each of these sets of connected structures, there are both reciprocal connections linking up regions associated with similar functions and non-reciprocal connections linking up regions that are associated with different cortical basal ganglia circuits. Each component of information (from limbic to motor outcome) sends both feedback connection, and also a feedforward connection, allowing the transfer of information. Information is channeled from limbic, to cognitive, to motor circuits. Action decision-making processes are thus influenced by motivation and cognitive inputs, allowing the animal to respond appropriate to environmental cues.

Integrity signals

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Reward information is processed via a limbic cortico-striatal-thalamic circuit that interdigitates with the mesolimbic DA pathway, and the NAc serves as a DA-gated mediator for information passing from the limbic system to the cortex.
“Reward information is processed via a limbic cortico-striatal-thalamic circuit that interdigitates with the mesolimbic DA pathway [56,57], and the NAc serves as a DA-gated mediator for information passing from the limbic system to the cortex [58].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [56]
Corticostriatal projections from agranular areas target the nucleus accumbens, and those from granular prefrontal areas terminate in the caudate nucleus.
“Corticostriatal projections from the agranular areas target the nucleus accumbens, and those from the granular prefrontal areas terminate in the caudate nucleus.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [131]
The reward circuitry is a distributed network classically described as part of the cortico-basal ganglia system.
“Briefly, the reward circuitry is a distributed network, classically described as part of the cortico-basal ganglia system (Alexander and Crutcher, 1990; Haber, 2003; Parent and Hazrati, 1995).”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Haber, 2003
The ACC is rich in dopamine receptors and recognized as a core node within the incentive motivational system, suggesting a possible neurochemical basis for the aggregation of regions that showed stronger activation likelihoods in adolescents relative to adults.
“Importantly, the ACC is rich in dopamine receptors and recognized as a core node within the incentive motivational system (Depue and Collins, 1999; Haber, 2003; Berridge, 2004), suggesting the possibility of a neurochemical basis for the aggregation of regions that showed stronger activation likelihoods in adolescents relative to adults.”
From Neural networks involved in adolescent reward processing: an activation likelihood estimation meta-analysis of functional neuroimaging studies (2015) · cites this paper as Haber, 2003
Highly processed cortical sensory inputs reach the ventral striatum through unidirectional projections from the insula and orbitofrontal cortex.
“Highly processed cortical sensory inputs reach the ventral striatum through unidirectional projections from the insula as well as from the orbitofrontal cortex (Haber, 2003).”
From Neural networks involved in adolescent reward processing: an activation likelihood estimation meta-analysis of functional neuroimaging studies (2015) · cites this paper as Haber, 2003

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Neurobiology of Aggression and Violence
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Distributed Neural Representation of Expected Value
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The organization of the human striatum estimated by intrinsic functional connectivity
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Schizophrenia, dopamine and the striatum: From biology to symptoms
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The short-latency dopamine signal: a role in discovering novel actions?
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Elevated Striatal Dopamine Function Linked to Prodromal Signs of Schizophrenia
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How Green Is the Grass on the Other Side? Frontopolar Cortex and the Evidence in Favor of Alternative Courses of Action
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The Nucleus Accumbens: Mechanisms of Addiction across Drug Classes Reflect the Importance of Glutamate Homeostasis
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Altered corticostriatal functional connectivity in obsessive-compulsive disorder
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The nucleus accumbens: a target for deep brain stimulation in obsessive-compulsive- and anxiety-disorders
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Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction
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Transient and Selective Overexpression of Dopamine D2 Receptors in the Striatum Causes Persistent Abnormalities in Prefrontal Cortex Functioning
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The neurobiology of depression and antidepressant action
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From dopamine to salience to psychosis—Linking biology, pharmacology and phenomenology of psychosis
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An automatic valuation system in the human brain: Evidence from functional neuroimaging
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Placebo and the New Physiology of the Doctor-Patient Relationship
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Efficacy and Safety of Deep Transcranial Magnetic Stimulation for Obsessive-Compulsive Disorder: A Prospective Multicenter Randomized Double-Blind Placebo-Controlled Trial
Carmi, L., Tendler, A., Bystritsky, A., Hollander, E., Blumberger, D. M., Daskalakis, J., Ward, H., Lapidus, K., Goodman, W., Casuto, L., et al. (2019) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.18101180 · Cited by 458 · see citing works
Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory
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Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks
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Toward a neurobiology of delusions
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Romantic love: a mammalian brain system for mate choice
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Romantic love: an fMRI study of a neural mechanism for mate choice.
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Corticostriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control
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The integrative function of the basal ganglia in instrumental conditioning
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The Functional Neuroanatomy of Maternal Love: Mother’s Response to Infant’s Attachment Behaviors
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The mouse cortico–basal ganglia–thalamic network
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Cortico-Striatal-Thalamic Loop Circuits of the Orbitofrontal Cortex: Promising Therapeutic Targets in Psychiatric Illness
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The role of the striatum in social behavior
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Neural mechanisms underlying motivation of mental versus physical effort
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Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings
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Specific frontostriatal circuits for impaired cognitive flexibility and goal-directed planning in obsessive-compulsive disorder: Evidence from resting-state functional connectivity
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L-dopa modulates functional connectivity in striatal cognitive and motor networks: A double-blind placebo-controlled study
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Abnormally high degree connectivity of the orbitofrontal cortex in obsessive-compulsive disorder
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Neural networks involved in adolescent reward processing: an activation likelihood estimation meta-analysis of functional neuroimaging studies
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Neural Hyporesponsiveness and Hyperresponsiveness During Immediate and Delayed Reward Processing in Adult Attention-Deficit/Hyperactivity Disorder
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A Proposal for a Coordinated Effort for the Determination of Brainwide Neuroanatomical Connectivity in Model Organisms at a Mesoscopic Scale
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Presynaptic Striatal Dopamine Dysfunction in People at Ultra-high Risk for Psychosis: Findings in a Second Cohort
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Similar roles of substantia nigra and ventral tegmental dopamine neurons in reward and aversion
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From ventral-medial to dorsal-lateral striatum: neural correlates of reward-guided decision-making
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Dopaminergic basis of salience dysregulation in psychosis
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Frontoparietal areas link impairments of large-scale intrinsic brain networks with aberrant fronto-striatal interactions in OCD: a meta-analysis of resting-state functional connectivity
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Dopamine Transmission in the Human Striatum during Monetary Reward Tasks
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Brain corticostriatal systems and the major clinical symptom dimensions of obsessive-compulsive disorder
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“The expected free energy is computed in the medial prefrontal cortex [44] during planning, which leads to inferences about most plausible policies (decisionmaking) in the basal ganglia, consistent with the fact that the basal ganglia is thought to underwrite planning and decision-making [166–171].”
Result
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Relationship of resting brain hyperconnectivity and schizophrenia-like symptoms produced by the NMDA receptor antagonist ketamine in humans
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Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala
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Neurocognitive mechanisms of action control: resisting the call of the Sirens.
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Fronto-striatal organization: defining functional and microstructural substrates of behavioural flexibility
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Authors: Haber, S. N.
Affiliations: University of Rochester Medicine (US)
Corresponding author: Haber, Suzanne N.
ORCID: Haber, Suzanne N.
Venue: Journal of Chemical Neuroanatomy
Publisher: Elsevier BV
Published: 2003-12
Volume: 26
Issue: 4
Pages: 317-330
ISSN: 0891-0618 (ISSN-L)
DOI: 10.1016/j.jchemneu.2003.10.003
OpenAlex: W2150857753
Cited by: 1,479
References: 206
Citations by year: 2026: 33 · 2025: 41 · 2024: 55 · 2023: 55 · 2022: 56 · 2021: 87 · 2020: 77 · 2019: 69 · 2018: 79 · 2017: 83 · 2016: 77 · 2015: 85 · 2014: 93 · 2013: 85 · 2012: 92
FWCI: 2.94
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Chemical Neuroanatomy (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (n44ns022311-002)
National Institute of Mental Health (MH45573)
National Institute of Neurological Disorders and Stroke (NS22311)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Health Sciences › Medicine › Neurology › Neurological disorders and treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: basal ganglia, frontal cortex, primate neuroanatomy, parallel neural pathways, goal-directed behavior, motivation, basal ganglia circuitry
MeSH terms: Animals, Basal Ganglia, Humans, Mental Processes, Neural Pathways, Primates

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The primate basal ganglia: Parallel and integrative networks

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