How do cortico-striatal projections impact on downstream pallidal circuitry?
The frontal cortico-basal ganglia network plays a central role in action selection, associative learning, and motivation, processes requiring the integration of information from functionally distinct cortical regions. The cortico-striatal projection is a likely substrate of information integration, as terminal fields from different cortical regions converge in the striatum. These intersecting projections form complex zones of unique cortical inputs. Here, our goal was to follow these projection zones downstream in the basal ganglia to the globus pallidus. We combined a sizable database of 3D models of striato-pallidal chartings in macaques with maps of frontal cortical inputs to determine the topography of the striato-pallidal projection and the indirect cortical influence over the pallidum. We found that the striato-pallidal projection is highly topographic, with the location of the striatal injection site strongly predicting the location of the resulting pallidal terminal fields. Furthermore, striato-pallidal projections are specific and largely nonoverlapping. Thus, striatal hubs receiving unique combinations of cortical inputs have distinct projections to the pallidum. However, because of the strong convergence of cortical terminal fields in the striatum, the indirect pallidal representation of any given frontal cortical region remains broad. We illustrate this arrangement by contrasting the pallidal projections from two nearby striatal cases: one a putative hub for cortical attentional bias signals, and the other with a different, more ventral set of cortical inputs. Thus, the striato-pallidal projection faithfully conveys unique combinations of cortical inputs to different locations within the pallidum via the striatum.
KeywordsBasal ganglia Prefrontal cortex Globus pallidus Striatum
This work was supported by Grant nos. R01MH045573, P50MH086404 (SNH), F32MH103931, and a Tourette Syndrome Postdoctoral Fellowship (SRH). The authors declare no competing financial interests.
Compliance with ethical standards
Conflict of interest
The authors declare no conflicts of interest.
Human and animal rights
Animal research was approved by the University Committee on Animal Resources at the University of Rochester Medical Center and was conducted according to the Guide for the Care and Use of Laboratory Animals.
- Calzavara R, Mailly P, Haber SN (2007) Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: an anatomical substrate for cognition to action. Eur J Neurosci 26:2005–2024. https://doi.org/10.1111/j.1460-9568.2007.05825.x CrossRefPubMedPubMedCentralGoogle Scholar
- Carpenter MB (1976) Anatomical organization of the corpus striatum and related nuclei. In: Yahr MD (ed) The Basal Ganglia. Raven Press, New York, pp 1–36Google Scholar
- DeLong MR, Georgopoulos AP, Crutcher MD et al (1984) Functional organization of the basal ganglia: contributions of single-cell recording studies. In: Functions of the basal ganglia. Pitman, London, pp 64–82Google Scholar
- Fox CH, Andrade HN, Du Qui IJ, Rafols JA (1974) The primate globus pallidus. A Golgi and electron microscope study. J R Hirnforsch 15:75–93Google Scholar
- Haber SN, Kim KS, Mailly P, Calzavara R (2006) Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26:8368–8376. https://doi.org/10.1523/JNEUROSCI.0271-06.2006 CrossRefPubMedGoogle Scholar
- Melendez RI, Rodd-Henricks ZA, McBride WJ, Murphy JM (2003) Alcohol stimulates the release of dopamine in the ventral pallidum but not in the globus pallidus: a dual-probe microdialysis study. Neuropsychopharmacology 28:939–946. https://doi.org/10.1038/sj.npp.13000811300081 CrossRefPubMedGoogle Scholar
- Parent A, Hazrati L-N, Charara A et al (1997) The striatopallidal fiber system in primates. In: Obeso MR, Ohye C, Marsden CDJD (eds) The basal ganglia and new surgical approaches for Parkinson’s disease, advances in neurology. Lippincott-Raven, Philadelphia, pp 19–29Google Scholar
- Percheron G, Francois C, Yelnik J, Fenelon G (1989). The primate nigro-striato-pallido-nigral system. Not a mere loop. Neural Mechanisms in Disorders of Movement, pp 103–109Google Scholar