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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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“putamen, substantia nigra, and the thalamus (Alexander, 1986; Aron et al., 2007; Chudler & Dong, 1995; Middleton, 2002), making it reasonable to propose that left DLPFC stimulation modulates the sensorimotor cortical excitability through its effects on subcortical regions (Fierro et al.”
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“Still, the identification of extensive functional connections between the striatum and non-motor cortical areas (13, 14) raised the hypothesis of an involvement of the basal ganglia also in associative, cognitive and emotional processes.”
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“…receives reward-related information from striatum and outputs directly to motor-related structures such as superior colliculus as well as to thalamus, which projects to cortical areas such as motor cortex and prefrontal cortex (Deniau et al., 1994; Hoover & Strick, 1999; Middleton & Strick, 2002).”
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“…including the striatum, the subthalamic nucleus and the globus pallidus pars externa and projects primarily to ventral anterior and lateral nuclei of the thalamus, indirectly connecting with cortical sites (Hoover and Strick, 1993; Middleton and Strick, 1994, 2002; Parent and Hazrati, 1995).”
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“This channel-based scheme is consonant with the view that the basal ganglia comprise a series of afferent and efferent parallel processing streams or loops (Alexander et al. 1986; Hoover & Strick 1993; Middleton & Strick 2002).”
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“Additionally, the frontal cor tex receives the largest portion of BG outputs, suggesting a close collaboration between these structures (Middleton and Strick, 1994,2000,2002).”
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“These functions are typically associated with the frontal (Alvarez & Emory, 2006) and prefrontal cortex, thalamus, basal ganglia (Middleton & Strick, 2002) and parietal portions of the brain(Colcombe et al., 2004).”
BackgroundTremblay, L., Worbe, Y., & Hollerman, J. R. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374620-7.00003-0 · Cited by 32
A hypothetical role of cortico-basal ganglia-thalamocortical loops in visual processing
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“The BG nuclei are part of topographically closed cortico-BG-thalamocortical (C-BG-Th-C) loops, since the targeted cortical area (visual or prefrontal) is both a target of the BG output and a source of input to the BG (Middleton and Strick, 1996, 2002) (Fig.”
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“According to the topographical map of the GPi, this region appears to be located just caudal to the association territory (Middleton & Strick, 2002; Akkal et al., 2007), suggesting that it is situated in the transition zone between motor and association territories, which represent the…”
BackgroundInfluentialMotor Areas in the Frontal Lobe
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Adaptations of glutamatergic synapses in the striatum contribute to recovery from cerebellar damage
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“…loop and cortico-basal ganglia-thalamo-cortical loop are differently engaged in motor skill acquisition and execution (Friston et al., 1992; Grafton, 1994; Jenkins et al., 1994; Seitz et al., 1994; Jueptner et al., 1997; Toni et al., 1998; Middleton & Strick, 2002).”
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“The premotor regions with the thalamus and striatum form the cortico-striato-thalamo-cortical circuits (Middleton and Strick, 2002), and are known to actively communicate during speed emphasized tasks (Van Veen et al.”
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“…animal work showing that the caudate nucleus and putamen receive cortical projections and project back to cortical regions via the thalamus, forming parallel [Middleton and Strick, 2002] and integrative circuits in support of motor, cognitive, and emotional processes [Bar-Gad and Bergman, 2001].”
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“Some data have suggested changes in PFC functions and innervation patterns with the latter direction of modulation (Deniau et al., 1994; Kitabatake et al., 2003; Middleton and Strick, 2002).”
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“Animal work has shown that the caudate nucleus and the putamen receive cortical projections and project back to cortical regions via the thalamus, forming parallel [Middleton and Strick, 2002] and integrative [Bar-Gad and Bergman, 2001] circuits in support of motor, cognitive, and emotional processes.”
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“Cortico-striato-thalamo-cortical loops, which involve various subdivisions of the PFC, are then used to project thalamic and Gpi/SNr outputs back to cortical areas (2, 172, 303, 432).”
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“GPi and SNr innervate specific and different parts of PFC, and these connections are segregated from GPi and SNr neurons that innervate the motor cortex (Middleton and Strick 2002).”
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“Middleton and Strick (2002) found that the cognitive and motor pathways of the GPi/SNr-thalamus-cortex are segregated and that DLPFC is a target of BG output.”
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“Middleton and Strick [91], reported that about one-third of the total output from the basal ganglia is directed to the medial and lateral area 9, dorsal and ventral area 46 and lateral area 12 of the prefrontal”
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BackgroundMeier, B., Weiermann, B., Gutbrod, K., Stephan, M. A., Cock, J. J., Müri, R. M., & Kaelin‐Lang, A. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2013.10.009 · Cited by 20
Prefrontal cortical thinning in HIV infection is associated with impaired striatal functioning
du Plessis, S., Vink, M., Joska, J. A., Koutsilieri, E., Bagadia, A., Stein, D. J., & Emsley, R. A. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1571-0 · Cited by 21
“This is based on anatomical (Middleton and Strick 2002), functional connectivity (Zandbelt and Vink 2010) and probabilistic tracking studies (Draganski et al.”
Herold, C., Diekamp, B., & Güntürkün, O. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.07.017 · Cited by 23
“Both areas are highly connected via the prefronto-striatal loop [2,15,58].”
Neuronal basis for evaluating selected action in the primate striatum
Yamada, H., Inokawa, H., Matsumoto, N., Ueda, Y., & Kimura, M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07771.x · Cited by 21
“11), where signals from the ACC, medial and dorsolateral prefrontal, and orbitofrontal cortices project (Middleton & Strick, 2002; Haber et al., 2006).”
BackgroundWilson, C. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.025 · Cited by 20
“The segregation of motor and nonmotor regions of the dorsal striatum is preserved in the striatal outflow to the output nuclei of the basal ganglia, thalamic connections, and cortical targets (Middleton and Strick, 2002).”
BackgroundBrown, M. J. N., Goldenkoff, E. R., Chen, R. E., Gunraj, C. A., & Vesia, M. (2019) · Brain Sciences · doi:10.3390/brainsci9080177 · Cited by 19
“DLPFC also is known to have reciprocal connections with the basal ganglia [12,62,63] and connections to various motor nuclei within the thalamus [7,64–66].”
BackgroundBartolo, P. D., Gelfo, F., Burello, L., Giorgio, A. D., Petrosini, L., & Granato, A. (2011) · The Cerebellum · doi:10.1007/s12311-011-0275-0 · Cited by 20
“Therefore, it has been hypothesized that two separate networks support the different involvement of the two regions in motor control: the cortico-ponto-cerebello-thalamo-cortical loop and the cortico-basal ganglia-thalamo-cortical loop [1, 2, 4, 5, 10, 11 ].”
BackgroundA four-year prospective study of cognitive functioning in Huntington's disease
Ward, J., Sheppard, J. E., Shpritz, B., et al. (2006) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617706060565 · Cited by 20
Altered Functional Connectivity of Striatal Subregions in Patients with Multiple Sclerosis
Cui, F., Zhou, L., Wang, Z., Lang, C., Park, J., Tan, Z., Yu, Y., Sun, C., Gao, Y., & Kong, J. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00129 · Cited by 20
“Curr Opin Neurobiol (2007) 17(2):234–42.”
MethodResultInfluentialRapid eye movement sleep behavior disorder
Chen, M. C., Yu, H., Huang, Z., & Lu, J. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.02.019 · Cited by 19
“Another possibility is that differences in basal ganglia projection patterns to premotor and primary motor regions [51] resolve premotor dysfunction during REM sleep (Figure 2c).”
BackgroundReward network dysfunction is associated with cognitive impairment after stroke
Wagner, F., Rogenz, J., Opitz, L., Maas, J., Schmidt, A., Brodoehl, S., Ullsperger, M., & Klingner, C. M. (2023) · NeuroImage Clinical · doi:10.1016/j.nicl.2023.103446 · Cited by 19
“These studies have found an association between stroke lesions in key anatomical structures of the reward system and post stroke depression as also clinically apparent apathy (Narushima et al., 2003; Rochat et al., 2013).”
Licea, J., Khan, O., Singh, T., & Modlesky, C. M. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.16211 · Cited by 19
“While not directly involved in motor command execution, the PFC has extensive connections with cortical and subcortical motor areas (Middleton & Strick, 2002) that allow it to exert significant influence over motor performance (Bigliassi & Filho, 2022).”
Activity of neurons in the caudate and putamen during a visuomotor task
Romero, M. C., Bermúdez, M. A., Vicente, A. F., Perez, R., & González, F. (2008) · Neuroreport · doi:10.1097/wnr.0b013e328307c3fc · Cited by 19
Cholinergic innervation of the basal ganglia in humans and other anthropoid primates
Stephenson, A. R., Edler, M. K., ERWIN, J. M., Jacobs, B., Hopkins, W. D., Hof, P. R., Sherwood, C. C., & Raghanti, M. A. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24067 · Cited by 21
“The nuclei of the basal ganglia are topographically organized to influence the cognitive processes of the frontal lobe (Parent and Hazrati, 1995; Wise et al., 1996; Hardman et al., 2002; Middleton and Strick, 2002).”
BackgroundFazio, L., Logroscino, G., Taurisano, P., Amico, G., Quarto, T., Antonucci, L. A., Barulli, M. R., Mancini, M., Gelao, B., Ferranti, L., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165301 · Cited by 20
The Basal Ganglia and Language: A Tale of Two Loops
Bohsali, A. A., & Crosson, B. (2016) · Innovations in cognitive neuroscience · doi:10.1007/978-3-319-42743-0_10 · Cited by 20
Age-Related Influences of Prior Sleep on Brain Activation during Verbal Encoding
Jonelis, M. B., Drummond, S. P. A., Salamat, J. S., et al. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00049 · Cited by 18
“Although the general trend is toward a decline with age, OLD show greater variability than YOUNG in both sleep and cognition, with some OLD showing little or no decline relative to YOUNG (Middleton and Strick, 2002; Ohayon et al., 2004).”
BackgroundEffect of memantine on CBF and CMRO2in patients with early Parkinson’s disease
Borghammer, P., Vafaee, M. S., Østergaard, K., et al. (2007) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2007.00943.x · Cited by 18
“More than one-third of the output from GPi and SNr projects to these areas (26).”
BackgroundMartins, R., Simard, F., Provost, J.-S., & Monchi, O. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr222 · Cited by 19
“The WWST is a lexical analog of the computerized WCST used by Monchi et al. (2001), in which French words are used instead of the usual pictogram cards.”
MethodTropea, T. F., Guerriero, R. M., Willuhn, I., et al. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.12.002 · Cited by 18
Brain Networks Sensitive to Object Novelty, Value, and Their Combination
Ghazizadeh, A., Fakharian, M. A., Amini, A., Griggs, W. S., Leopold, D. A., & Hikosaka, O. (2020) · Cerebral Cortex Communications · doi:10.1093/texcom/tgaa034 · Cited by 18
Ghazizadeh, A., & Hikosaka, O. (2021) · Science Advances · doi:10.1126/sciadv.abe0693 · Cited by 16
Psychological and Neuroscientific Connections with Reinforcement Learning
Shah, A. (2012) · Adaptation, learning, and optimization · doi:10.1007/978-3-642-27645-3_16 · Cited by 17
Problems and Solutions for Circuits and Synapses in Parkinson's Disease
Ole Isacson, A. (2004) · Neuron · doi:10.1016/j.neuron.2004.07.007 · Cited by 16
Ventrolateral Prefrontal Cortex Contributes to Human Motor Learning
Kumar, N., Sidarta, A., Smith, C. E., & Ostry, D. J. (2022) · eNeuro · doi:10.1523/eneuro.0269-22.2022 · Cited by 16
“Outputs from the basal ganglia to area 9/46v have also been reported (Middleton and Strick, 2002).”
BackgroundMathematical expertise modulates the architecture of dorsal and cortico-thalamic white matter tracts
Jeon, H., Kuhl, U., & Friederici, A. D. (2019) · Scientific Reports · doi:10.1038/s41598-019-43400-6 · Cited by 16
Maxwell, J. R., Zimmerman, A. J., Pavlik, N. G., Newville, J., Carlin, K., Robinson, S., Brigman, J. L., Northington, F. J., & Jantzie, L. L. (2020) · Frontiers in Pediatrics · doi:10.3389/fped.2020.00289 · Cited by 16
“The efficient balance of associative learning and behavioral flexibility is mediated by cortico-striatal-thalamic loops (54) and single unit recording and imaging studies have demonstrated that the striatum plays a critical role in the representation of rewardaction relationships required to efficiently guide choices…”
BackgroundOn the Role of Dopamine in Cognitive Vision
Vitay, J., & Hamker, F. H. (2007) · Lecture notes in computer science · doi:10.1007/978-3-540-77343-6_23 · Cited by 16
“This information can then be sent back to prefrontal cortex through direct connections between the striatum and the mediodorsal part of the thalamus [60] and/or indirectly through GPi.”
BackgroundScholl, C., Baladron, J., Vitay, J., & Hamker, F. H. (2022) · Brain Structure and Function · doi:10.1007/s00429-021-02446-x · Cited by 16
“A so-called associative circuit was localized in the dorsomedial striatum (caudate nucleus), which receives its inputs from the prefrontal cortex (Alexander et al. 1986; Alexander and Crutcher 1990; Middleton and Strick 2002).”
BackgroundTurk, K. W., Flanagan, M. E., Josephson, S., Keene, C. D., Jayadev, S., & Bird, T. D. (2017) · The Cerebellum · doi:10.1007/s12311-017-0882-5 · Cited by 15
Neuropsychological Functioning in Primary Dystonia: Updated and Expanded Multidomain Meta‐Analysis
Aita, S. L., Bene, V. A. D., Marotta, D. A., Pizer, J. H., Hawley, N. A., Niccolai, L. M., Walker, H. C., Gerstenecker, A. T., Martin, R. C., Clay, O. J., et al. (2022) · Movement Disorders · doi:10.1002/mds.29022 · Cited by 15
Storvik, M., Arguel, M., Schmieder, S., et al. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.02.008 · Cited by 15
“As the PFC receives massive projections from the basal ganglia (Middleton and Strick, 2002), detecting the ongoing degeneration is most likely conveyed by the network and thus by changes in electrophysiological activity.”
BackgroundInfluential
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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