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Basal-ganglia 'Projections' to the Prefrontal Cortex of the Primate
Abstract
We used retrograde transneuronal transport of the McIntyre-B strain of herpes simplex virus type 1 to examine the extent and organization of basal-ganglia-thalamocortical projections to five regions of prefrontal cortex in the cebus monkey (Cebus apella): medial and lateral area 9 (9m and 9l), dorsal and ventral area 46 (46d and 46v) and lateral area 12 (12l). All of these prefrontal areas were found to be targets of basal-ganglia output that originated in the internal segment of the globus pallidus (GPi) and/or the pars reticulata of the substantia nigra (SNpr). Approximately one-third of the total volume of these nuclei was directed toward prefrontal cortex, a volume comparable to that directed at the cortical motor areas. The origins of the outputs to different prefrontal areas were topographically organized. Different portions of SNpr (the rostral and caudal thirds) projected to areas 9m and 12l. Similarly, different output nuclei (GPi and SNpr) projected to adjacent portions of the same cytoarchitectonic field (46d and 46v). Furthermore, the outputs to prefrontal areas were segregated from those to motor areas of cortex. Thus, basal-ganglia outputs to prefrontal cortex are both extensive and topographically organized, forming a rich anatomical substrate for basal-ganglia influences on the cognitive operations of the frontal lobe.
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“These patterns of size-independently co-evolving brain structures correspond to brain systems that have been described in electrophysiological and anatomical tract-tracing studies in non-human primates [27–31] and MRI studies in humans [32–35]”
From Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution (2013) · cites this paper as [27]
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“…2002; Leerkes et al., 2008), b) the neuroanatomical patterns of prefrontal connectivity as the nexus of the limbic and attention systems (e.g., Middleton & Strick, 2002; Pandya & Yeterian, 1996), c) the emerging evidence of interactions among executive and emotional task demands (e.g., Zelazo…”
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“Much less is known about the role of the BG, with which these cortical regions are tightly linked (Alexander et al., 1986; Middleton and Strick, 2002).”
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Worbe, Y., Baup, N., Grabli, D., Chaigneau, M., Mounayar, S., McCairn, K. W., Féger, J., & Tremblay, L. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn214 · Cited by 183
GluN2B in corticostriatal circuits governs choice learning and choice shifting
Brigman, J. L., Daut, R. A., Wright, T., Gunduz‐Cinar, O., Graybeal, C., Davis, M. I., Jiang, Z., Saksida, L. M., Jinde, S., Pease, M. W., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3457 · Cited by 162
Thalamic mechanisms in language: A reconsideration based on recent findings and concepts
Crosson, B. (2012) · Brain and Language · doi:10.1016/j.bandl.2012.06.011 · Cited by 175
“Controlled processing is likely to involve frontal cortices, which are more consistently involved in basal ganglia loops than other cortical regions (Middleton & Strick, 2000, 2002).”
Evolution of the basal ganglia: Dual‐output pathways conserved throughout vertebrate phylogeny
Stephenson‐Jones, M., Ericsson, J., Robertson, B., & Grillner, S. E. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23087 · Cited by 165
“The GPi projects via the thalamus to areas of the cortex that influence cognitive functions as well as movements and also directly to brainstem nuclei (Akkal et al., 2007; Kelly and Strick, 2004; Middleton and Strick, 2002).”
BackgroundSubcortical contributions to large-scale network communication
Bell, P. T., & Shine, J. M. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.036 · Cited by 168
Different activation patterns for working memory load and visual attention load
Tomasi, D. G., Chang, L., Caparelli, E. C., & Ernst, T. (2006) · Brain Research · doi:10.1016/j.brainres.2006.11.030 · Cited by 163
“Such connections are supported by studies in non-human primates showing that the thalamus (Middleton, 2000, Middleton and Strick, 2002) and the IPL (Clower et al., 2001) receive projections from many brain regions Findings of higher cross-correlation of load-related BOLD responses during VA tasks…”
BackgroundRomanelli, P., Esposito, V., Schaal, D. W., & Heit, G. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.09.008 · Cited by 168
A dopaminergic basis for working memory, learning and attentional shifting in Parkinsonism
Moustafa, A. A., Sherman, S. J., & Frank, M. J. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.07.011 · Cited by 192
“…in the cognitive domain, the G serve as a gate to modulate when and when not to update inforation into prefrontal cortex (Frank et al., 2001; Middleton & Strick, 000; Middleton & Strick, 2002; O’Reilly & Frank, 2006), to be mainained in an active state, forming the basis of WM (Goldman-Rakic, 995).”
BackgroundExtrastriatal dopaminergic circuits of the basal ganglia
Rommelfanger, K. S. (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00139 · Cited by 166
Compromised fronto-striatal functioning in HIV: An fMRI investigation of semantic event sequencing
Melrose, R. J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.021 · Cited by 148
Basal ganglia and language: phonology modulates dopaminergic release
Tettamanti, M., Moro, A., Messa, C., Moresco, R. M., Rizzo, G., Carpinelli, A., Matarrese, M., Fazio, F., & Perani, D. (2005) · Neuroreport · doi:10.1097/00001756-200503150-00018 · Cited by 146
“INTRODUCTION Strong evidence for the role of basal ganglia in cognition has come from research in primates, showing that the basal ganglia are interconnected by input and output fibers with the frontal lobe [1].”
BackgroundBilateral basal ganglia activation associated with sensorimotor adaptation
Seidler, R. D., Noll, D. C., & Chintalapati, P. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0571-y · Cited by 145
“Recent anatomical studies have demonstrated a connection between the globus pallidus and the prefrontal cortex, including BA 46 (Middleton and Strick 2002; Kelly and Strick 2004).”
BackgroundLü, Y., Liang, H., Han, D., Mo, Y., Li, Z., Cheng, Y., Xu, X., Shen, Z., Tan, C., Zhao, W. D., et al. (2016) · NeuroImage Clinical · doi:10.1016/j.nicl.2016.04.008 · Cited by 149
“According to previous studies, sensory, motor and cognitive processes are organised and integrated in distinct nuclei of the thalamus, which have connections with specific cortical and subcortical regions (Alexander et al., 1986; Middleton and Strick, 2002).”
MethodMa, L., Wang, B., Narayana, S., Hazeltine, E., Chen, X., Robin, D. A., Fox, P. T., & Xiong, J. (2010) · Brain Research · doi:10.1016/j.brainres.2009.12.073 · Cited by 146
The macaque lateral grasping network: A neural substrate for generating purposeful hand actions
Borra, E., Gerbella, M., Rozzi, S., & Luppino, G. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.017 · Cited by 149
Tai Chi Chuan and Baduanjin Increase Grey Matter Volume in Older Adults: A Brain Imaging Study
Tao, J., Liu, J., Liu, W., Huang, J., Xue, X., Chen, X., Wu, J., Zheng, G., Chen, B., Li, M., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170477 · Cited by 143
“Thecontributionoftheputamenincognitionmay beduetotheexistenceofcircuitsconnectingthe basalgangliatonon-motorregionsinthefrontallobe [82]thatareassociatedwithavarietyofcognitive functions[83].”
Cell-based reporters reveal in vivo dynamics of dopamine and norepinephrine release in murine cortex
Muller, A., Joseph, V., Slesinger, P. A., & Kleinfeld, D. (2014) · Nature Methods · doi:10.1038/nmeth.3151 · Cited by 139
Development of Working Memory Maintenance
Geier, C. F., Garver, K., Terwilliger, R., & Luna, B. (2009) · Journal of Neurophysiology · doi:10.1152/jn.90562.2008 · Cited by 136
Transneuronal Circuit Analysis With Pseudorabies Viruses
Card, J. P., & Enquist, L. W. (1999) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0105s09 · Cited by 135
Quantitative cerebral water content mapping in hepatic encephalopathy
Shah, N. J., Neeb, H., KIRCHEIS, G., et al. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.02.057 · Cited by 132
“…to the water content as a marker for abnormal coupling with regions attributable to the frontal corticalbasal ganglia circuits (Middleton and Strick, 1994; Rolls, 1994; Brown et al., 1997; Haber and McFarland, 2001; McFarland and Haber, 2002; Middleton and Strick, 2002; Kelly and Strick, 2003).”
InfluentialHow the motor system integrates with working memory
Marvel, C. L., Morgan, O. P., & Kronemer, S. I. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.04.017 · Cited by 142
Marchand, W. R. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0280-y · Cited by 137
“Other studies have shown that there is segregation of striatopallidal projections (Hazrati and Parent 1992a, b) and that pallidal output is organized into discrete channels (Hoover and Strick 1993; Middleton and Strick 2002).”
BackgroundAction-verb processing in Parkinson’s disease: new pathways for motor–language coupling
Cardona, J. F., Gershanik, O. S., Gelormini‐Lezama, C., Houck, A. L., Cardona, S., Kargieman, L., Trujillo, N., Arévalo, A. L., Amoruso, L., Manes, F. F., et al. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0510-1 · Cited by 140
“The BG have profuse connections with the cerebral cortex, particularly with the frontal lobes (Middleton and Strick 2000, 2002; Ullman 2006).”
BackgroundRole of Individual Basal Ganglia Nuclei in Force Amplitude Generation
Spraker, M. B., Yu, H., Corcos, D. M., & Vaillancourt, D. E. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00239.2007 · Cited by 133
Annotation: Tourette syndrome: a relentless drumbeat – driven by misguided brain oscillations
Leckman, J. F., Vaccarino, F. M., Kalanithi, P. S. A., & Rothenberger, A. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01620.x · Cited by 136
Mailly, P., Charpier, S., Menetrey, A., & Deniau, J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05247.2003 · Cited by 129
“…premotor networks and thalamic nuclei related to motor , premotor, prefrontal, and associative sensory cortical areas (Deniau and Chevalier, 1992; Middleton and Strick, 1996, 2002; Sakai et al., 1998) (for review, see also Alexander et al., 1986; Parent, 1990; Deniau and Thierry, 1997; Bolam et…”
BackgroundBasal ganglia mechanisms underlying precision grip force control
Prodoehl, J., Corcos, D. M., & Vaillancourt, D. E. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.03.004 · Cited by 130
“…the motor cortex (Akkal et al., 2007;Clower et al., 2005;Hoover and Strick, 1999;Middleton and Strick, 2000), prefrontal cortex (Middleton and Strick, 1994;Middleton and Strick, 2002), and temporal lobe (Middleton and Strick, 1996), the output of the basal ganglia clearly targets the parietal lobe.”
BackgroundNeuroanatomy of Reward: A View from the Ventral Striatum
Haber, S. N. (2011) · Europe PMC (PubMed Central) · Cited by 125
Motor sequence chunking is impaired by basal ganglia stroke
Boyd, L. A., Edwards, J. D., Siengsukon, C. F., Vidoni, E. D., Wessel, B., & Linsdell, M. A. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.02.009 · Cited by 125
What Can Different Motor Circuits Tell Us About Psychosis? An RDoC Perspective
Mittal, V. A., Bernard, J. A., & Northoff, G. (2017) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx087 · Cited by 126
“By governing the selection or gating of a subset of representations that have been activated by the cortex, parallel basal ganglia circuits are responsible for modulating a range of higher order behaviors.[4,5] Basal ganglia circuits each share the same general organization, originating in specific cortical areas, pas…”
Metadata
- Authors
- Middleton, F. A.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- Middleton, F. A.
- ORCID
- Middleton, F. A.
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-09-01
- Volume
- 12
- Issue
- 9
- Pages
- 926-935
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2142455573
- Semantic Scholar
- 694a295bee8ec9996ffe86fdc9c06d779f885fdf
- Cited by
- 451
- References
- 58
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 5 · 2023: 9 · 2022: 14 · 2021: 12 · 2020: 13 · 2019: 8 · 2018: 20 · 2017: 18 · 2016: 27 · 2015: 20 · 2014: 19 · 2013: 22 · 2012: 33
- FWCI
- 11.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5f31mh011262-02)
- National Institute of Mental Health (R01MH056661, MH11262, MH-56661)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- basal ganglia, prefrontal cortex, thalamocortical connections, globus pallidus internus, substantia nigra pars reticulata, topographic organization, Cebus apella, area 46, retrograde tracing, herpes simplex virus type 1
- MeSH terms
- Animals, Axonal Transport, Basal Ganglia, Cebus, Neural Pathways, Prefrontal Cortex, Herpesvirus 1, Human
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