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 and MRI studies in humans.
“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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BackgroundBasal Ganglia and Cerebellar Inputs to ‘AIP’
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“This portion of SNpr also contains some neurons that project to regions of prefrontal cortex (Middleton and Strick, 2002).”
BackgroundVaillancourt, D. E., Thulborn, K. R., & Corcos, D. M. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00394.2003 · Cited by 237 · see citing works
Becker, D. R., Miao, A., Duncan, R. J., & McClelland, M. M. (2014) · Early Childhood Research Quarterly · doi:10.1016/j.ecresq.2014.04.014 · Cited by 240 · see citing works
“That is, there are anatomical connections between cerebellar and prefrontal cortices (Middleton & Strick, 2002), and evidence showing the cerebellum is active during EF tasks (Strick et al., 2009).”
BackgroundStriatocortical pathway dysfunction in addiction and obesity: differences and similarities
Tomasi, D. G., & Volkow, N. D. (2012) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2012.735642 · Cited by 232 · see citing works
Kelly, R. M., & Strick, P. L. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)43042-2 · Cited by 228 · see citing works
A Unified Model of Time Perception Accounts for Duration-Based and Beat-Based Timing Mechanisms
Teki, S., Grube, M., & Griffiths, T. D. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00090 · Cited by 229 · see citing works
“Frontiers in Integrative Neuroscience www.frontiersin.org January 2012 | Volume 5 | Article 90 | 4”
Working memory, attention, and salience in active inference
Parr, T., & Friston, K. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-15249-0 · Cited by 226 · see citing works
“However basal ganglia outputs also target sensory 62 and prefrontal 63 regions.”
BackgroundThe maturation of incentive processing and cognitive control
Geier, C., & Luna, B. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.01.021 · Cited by 225 · see citing works
“The inter-connectivity of these brain regions has been well characterized (Alexander et al., 1986; Middleton and Strick, 1994; Middleton and Strick, 2000; Middleton and Strick, 2002; Carmichael and Price, 1995; Haber et al., 1995; Haber et al., 2000; Groenewegen et al., 1997).”
BackgroundDopamine depletion impairs frontostriatal functional connectivity during a set-shifting task
Nagano-Saito, A., Leyton, M., Monchi, O., Goldberg, Y. K., He, Y., & Dagher, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3921-07.2008 · Cited by 222 · see citing works
“The striatum receives abundant projections from the frontal lobe (Alexander et al., 1986; Middleton and Strick, 2000, 2002).”
BackgroundBirdbrains could teach basal ganglia research a new song
DOUPE, A., PERKEL, D., REINER, A., & STERN, E. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.05.005 · Cited by 219 · see citing works
Selective dysfunction of basal ganglia subterritories: From movement to behavioral disorders
Tremblay, L., Worbe, Y., Thobois, S., Sgambato, V., & Féger, J. (2015) · Movement Disorders · doi:10.1002/mds.26199 · Cited by 212 · see citing works
Doyle, A., Faraone, S., Seidman, L. J., Willcutt, E., Nigg, J., Waldman, I., Pennington, B. F., Peart, J., & Biederman, J. (2005) · Journal of Child Psychology and Psychiatry and Allied Disciplines · doi:10.1111/j.1469-7610.2005.01476.x · Cited by 195 · see citing works
“Such areas have a high concentration of dopamine transporters (Anderson, Polcari, Lowen, Renshaw, & Teicher, 2002) and are connected to cortical loops that include the prefrontal cortex via the pons and other midbrain structures (Middleton & Strick, 2002).”
White matter structures associated with creativity: Evidence from diffusion tensor imaging
Takeuchi, H., Taki, Y., Sassa, Y., Hashizume, H., Sekiguchi, A., Fukushima, A., & Kawashima, R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.02.035 · Cited by 213 · see citing works
“The striatum receives abundant projections from the frontal lobe (Alexander et al., 1986; Middleton and Strick, 2000, 2002) and the dopaminergic system plays a role in the regulation of this corticostriatal (and thalamocortical) loop.”
BackgroundCauda, F., Cavanna, A. E., D’Agata, F., Sacco, K., Duca, S., & Geminiani, G. C. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2011.21624 · Cited by 208 · see citing works
“…of NAcc connectivity is mainly based on experimental studies using tractographic techniques in animals (Haber, Kim, Mailly, & Calzavara, 2006; Middleton & Strick, 1994, 2002; Ferry, Ongur, An, & Price, 2000; Haber, Fudge, &McFarland, 2000; Cavada &Goldman-Rakic, 1991; Selemon&GoldmanRakic,…”
The Functional Neuroanatomy of Temporal Discrimination
Pastor, M. A., Day, B. L., Macaluso, E., Friston, K. J., & Frackowiak, R. S. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4210-03.2004 · Cited by 209 · see citing works
“The latter are especially relevant, because they exert their effects on most components of the basal ganglia and their output centers (Smith et al., 1990; Parent and Hazrati, 1995; Middleton and Strick, 2002).”
BackgroundPalesi, F., Tournier, J., Calamante, F., Muhlert, N., Castellazzi, G., Chard, D., D'Angelo, E. U., & Wheeler‐Kingshott, C. A. M. G. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0861-2 · Cited by 205 · see citing works
“An additional observation is the presence of a conspicuous number of streamlines connecting the cerebellum to the basal ganglia via the RN and the thalamus (Middleton and Strick 2002).”
BackgroundMoran, A., Bergman, H., Israel, Z. H., & Bar‐Gad, I. (2008) · Brain · doi:10.1093/brain/awn270 · Cited by 206 · see citing works
Proactive inhibitory control of movement assessed by event-related fMRI
Jaffard, M., Longcamp, M., Velay, J., Anton, J., Roth, M., Nazarian, B., & Boulinguez, P. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.05.041 · Cited by 197 · see citing works
“It is likely that the basal ganglia–thalamocortical circuitry mediates this coupling (Alexander and Crutcher, 1990; Middleton and Strick, 2002; Mink, 1996).”
Dopamine modulation in the basal ganglia locks the gate to working memory
Gruber, A. J., Dayan, P., Gutkin, B. S., & Solla, S. A. (2006) · Journal of Computational Neuroscience · doi:10.1007/s10827-005-5705-x · Cited by 189 · see citing works
“One possible route for this influence (Frank et al., 2001; Djurfeldt et al., 2001) is the prominent projections from ventral striatum to medial dorsal thalamus/PFC (Haber, 2003; Middleton and Strick, 2002; Groenewegen et al., 1997).”
BackgroundThe pars reticulata of the substantia nigra: a window to basal ganglia output
Deniau, J., Mailly, P., Maurice, N., & Charpier, S. (2007) · Progress in brain research · doi:10.1016/s0079-6123(06)60009-5 · Cited by 186 · see citing works
The primate working memory networks
Constantinidis, C., & Procyk, E. (2004) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.4.4.444 · Cited by 185 · see citing works
“The most recent reviews on prefrontal functions underline the importance of these facts (Duncan & Owen, 2000; Miller & Cohen, 2001; Paus, 2001).”
BackgroundHelms, G., Draganski, B., Frackowiak, R. S. J., Ashburner, J., & Weiskopf, N. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.03.053 · Cited by 181 · see citing works
“The basal ganglia receive projections from almost the entire cortex and channel output via thalamic relays (for a review see Graybiel, 1995; Haber, 2003; Middleton and Strick, 2002; © 2009 Elsevier Inc.”
Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements
Lynch, J. C., & Tian, J. (2005) · Progress in brain research · doi:10.1016/s0079-6123(05)51015-x · Cited by 182 · see citing works
Is Broca's Area Part of a Basal Ganglia Thalamocortical Circuit?
Ullman, M. T. (2006) · Cortex · doi:10.1016/s0010-9452(08)70382-4 · Cited by 183 · see citing works
Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards
Kim, H. F., & Hikosaka, O. (2015) · Brain · doi:10.1093/brain/awv134 · Cited by 181 · see citing works
“However, anatomical studies have suggested that each of these areas (e.g. SNr) receives topographically organized inputs from the striatum (François et al., 1994) and likewise sends topographic outputs (Parent, 1990; Hoover and Strick, 1999; Middleton and Strick, 2002).”
BackgroundExecutive control and dimensions of problem behaviors in preschool children
Espy, K. A., Sheffield, T. D., Wiebe, S. A., Clark, C. A. C., & Moehr, M. J. (2010) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02265.x · Cited by 179 · see citing works
“…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…”
Calzavara, R., Mailly, P., & Haber, S. N. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05825.x · Cited by 170 · see citing works
“The topographic organization of corticostriatal projections is, in general, considered to be related to different functional domains of the cortex (Middleton & Strick, 2002).”
BackgroundBack to front: cerebellar connections and interactions with the prefrontal cortex
Watson, T. C., Becker, N., Apps, R., & Jones, M. W. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00004 · Cited by 176 · see citing works
Kashani, A., Lepicard, E. M., Poirel, O., Videau, C., David, J. P., Fallet‐Bianco, C., Simon, A., Delacourte, A., Bruno Giros, A., Epelbaum, J., et al. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.04.010 · Cited by 175 · see citing works
“The prefrontal cortex (A9) is the target of massive intra-and subcortical afferents from almost all sensory modalities, motor cortex and thalamus (Middleton and Strick, 2002; Petrides and Pandya, 1999).”
BackgroundTemporal dynamics of basal ganglia response and connectivity during verbal working memory
Chang, C. E., Crottaz‐Herbette, S., & Menon, V. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.08.056 · Cited by 174 · see citing works
“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).”
Behavioral and Movement Disorders Induced by Local Inhibitory Dysfunction in Primate Striatum
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 169 · see citing works
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 165 · see citing works
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 167 · see citing works
“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 · see citing works
“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 163 · see citing works
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 · see citing works
“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 163 · see citing works
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 · see citing works
“…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 150 · see citing works
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 149 · see citing works
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 · see citing works
“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 146 · see citing works
“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 144 · see citing works
“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 141 · see citing works
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 143 · see citing works
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 139 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“…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 132 · see citing works
Marchand, W. R. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0280-y · Cited by 133 · see citing works
“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 144 · see citing works
“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 129 · see citing works
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 129 · see citing works
Mailly, P., Charpier, S., Menetrey, A., & Deniau, J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05247.2003 · Cited by 129 · see citing works
“…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 122 · see citing works
“…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 · see citing works
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 124 · see citing works
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 122 · see citing works
“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…”
- 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 › Neurology › Neurological disorders and treatments
- 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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