Basal Ganglia and Thalamic Contributions to Language Function: Insights from A Parallel Distributed Processing Perspective

Abstract

Cerebral representations are encoded as patterns of activity involving billions of neurons. Parallel distributed processing (PDP) across these neuronal populations provides the basis for a number of emergent properties: 1) processing occurs and knowledge (long term memories) is stored (as synaptic connection strengths) in exactly the same networks; 2) networks have the capacity for setting into stable attractor states corresponding to concepts, symbols, implicit rules, or data transformations; 3) networks provide the scaffold for the acquisition of knowledge but knowledge is acquired through experience; 4) PDP networks are adept at incorporating the statistical regularities of experience as well as frequency and age of acquisition effects; 5) networks enable content-addressable memory; 6) because knowledge is distributed throughout networks, they exhibit the property of graceful degradation; 7) networks intrinsically provide the capacity for inference. This paper details the features of the basal ganglia and thalamic systems (recurrent and distributed connectivity) that support PDP. The PDP lens and an understanding of the attractor trench dynamics of the basal ganglia provide a natural explanation for the peculiar dysfunctions of Parkinson’s disease and the mechanisms by which dopamine deficiency is causal. The PDP lens, coupled with the fact that the basal ganglia of humans bears strong homology to the basal ganglia of lampreys and the central complex of arthropods, reveals that the fundamental function of the basal ganglia is computational and involves the reduction of the vast dimensionality of a complex multi-dimensional array of sensorimotor input into the optimal choice from a small repertoire of behavioral options — the essence of reactive intention (automatic responses to sensory input). There is strong evidence that the sensorimotor basal ganglia make no contributions to cognitive or motor function in humans but can cause serious dysfunction when pathological. It appears that humans, through the course of evolution, have developed cortical capacities (working memory and volitional and reactive attention) for managing sensory input, however complex, that obviate the need for the basal ganglia. The functions of the dorsal tier thalamus, however, even viewed with an understanding of the properties of population encoded representations, remain somewhat more obscure. Possibilities include the enabling of attractor state constellations that optimize function by taking advantage of simultaneous input from multiple cortical areas; selective engagement of cortical representations; and support of the gamma frequency synchrony that enables binding of the multiple network representations that comprise a full concept representation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Modified from Percheron G, Yelnik J, François C. A Golgi analysis of the primate globus pallidus. III. Spatial organization of the striato-pallidal complex. Journal of Comparative Neurology. 1984;227:214–27; with permission. Put, putamen; PaL, globus pallidus externa; PaM, globus pallidus interna; Cd, caudate

Fig. 6
Fig. 7
Fig. 8

Abbreviations

Ach:

Acetylcholine

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid sodium ion channels

AOA:

Age of acquisition

Cm:

Centromedian nucleus of the thalamus

CNS:

Central nervous system

DBS:

Deep brain stimulation

DM:

Dorsomedial nucleus of the thalamus

GABA:

Gamma amino butyric acid

GPe:

Globus pallidus externa

GPi:

Globus pallidus interna

IML:

Internal medullary lamina of the thalamus

ITP:

Inferior thalamic peduncle

M1:

Primary motor cortex

MRF:

Midbrain reticular formation

MRI:

Magnetic Resonance Imaging

NE:

Norepinephrine

NMDA:

N-methyl-d-aspartate sodium-calcium-potassium ion channels

NR:

Nucleus reticularis of the thalamus

PAC:

Phase-amplitude coupling

PD:

Parkinson’s disease

PDP:

Parallel distributed processing

Pf:

Parafascicular nucleus of the thalamus

SMA:

Supplementary motor area

STN:

Subthalamic nucleus

SNpc:

Substantia nigra pars compacta

UPDRS:

United Parkinson’s Disease Rating Scale

V1, V2, V3, and V4:

Cortical visual areas

VLo:

Ventrolateral nucleus of the thalamus, pars oralis

References

  1. Alexander, G. E., Crutcher, M. D., & DeLong, M. R. (1990). Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Progress in Brain Research, 85, 119–146.

    CAS  PubMed  Article  Google Scholar 

  2. Aravena, P., Hurtado, E., Riveros, R., Cardona, J. F., Manes, F., & Ibáñez, A. (2010). Applauding with closed hands: neural signature of action-sentence compatibility effects. PLoS ONE, 5(7), e11751.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  3. Arcaro, M. J., Pinsk, M. A., & Kastner, S. (2015). The anatomical and functional organization of the human visual pulvinar. Journal of Neuroscience, 35, 9848–9871.

    CAS  PubMed  Article  Google Scholar 

  4. Baldassarre, G., Mannella, F., Fiore, V. C., Redgrave, P., Gurney, K., & Mirolli, M. (2013). Intrinsically motivated action-outcome learning and goal-based action recall: a system-level bio-constrained computational model. Neural Networks, 41, 168–187.

    PubMed  Article  Google Scholar 

  5. Bar-Gad, I., Morris, G., & Bergman, H. (2003). Information processing, dimensionality reduction and reinforcement learning in the basal ganglia. Progress in Neurobiology, 71, 439–473.

    PubMed  Article  Google Scholar 

  6. Behrmann, M., & Plaut, D. C. (2013). Distributed circuits, not circumscribed centers, mediate visual recognition. Trends in Cognitive Science, 17, 210–219.

    Article  Google Scholar 

  7. Benecke, R., Rothwell, J. C., Dick, J. P. R., Day, B. L., & Marsden, C. D. (1986). Performance of simultaneous movements in patients with Parkinson’s disease. Brain, 109, 739–757.

    PubMed  Article  Google Scholar 

  8. Benecke, R., Rothwell, J. C., Dick, J. P. R., Day, B. L., & Marsden, C. D. (1987). Disturbances of sequential movements in patients with Parkinsons disease. Brain, 110, 361–379.

    PubMed  Article  Google Scholar 

  9. Boulenger, V., Mechtouff, L., Thobois, S., Broussolle, E., Jeannerod, M., & Nazir, T. A. (2008). Word processing in Parkinson’s disease is impaired for action verbs but not for concrete nouns. Neuropsychologia, 46, 743–756.

    PubMed  Article  Google Scholar 

  10. Boulenger, V., Roy, A. C., Paulignan, Y., Déprez, V., Jeannerod, M., & Nazer, T. A. (2006). Cross-talk between language processes and overt motor behavior in the first 200 ms of processing. Journal of Cognitive Neuroscience, 18, 1607–1615.

    PubMed  Article  Google Scholar 

  11. Breedin, S., Saffran, E. M., & Coslett, H. B. (1994). Reversal of the concreteness effect in a patient with semantic dementia. Cognitive Neuropsychology, 11, 617–660.

    Article  Google Scholar 

  12. Breedin, S. D., & Martin, R. C. (1996). Patterns of verb impairment in aphasia: an analysis of four cases. Cognitive Neuropsychology, 13, 51–91.

    PubMed  Article  Google Scholar 

  13. Bridge, H., Leopold, D. A., & Bourne, J. A. (2016). Adaptive pulvinar circuitry supports visual cognition. Trends in Cogn Science, 20, 146–157.

    Article  Google Scholar 

  14. Churchland, P. S., & Sejnowski, T. J. (1992). The Computational Brain. Cambridge, Massachusetts: MIT Press.

    Google Scholar 

  15. Crabtree, J. W. (2018). Functional diversity of thalamic reticular subnetworks. Frontiers in Systems Neuroscience, 12 Article 41, 1–18.

  16. Crick, F. (1984). Function of the thalamic reticular complex: the searchlight hypothesis. Proceedings of the National Academy of Sciences USA, 81, 4586–4590.

    CAS  Article  Google Scholar 

  17. Crosson, B. (2013). Thalamic mechanisms in language: a reconsideration based on recent findings and concepts. Brain and Language, 126, 73–88.

    PubMed  Article  Google Scholar 

  18. Dagenbach, D., Kubat-Silman, A. K., & Absher, J. R. (2001). Human verbal working memory impairments associated with thalamic damage. International Journal of Neuroscience, 111, 67–87.

    CAS  Article  Google Scholar 

  19. Dalla Volta, R., Gianelli, C., Campione, G., & Gentilucci, M. (2009). Action word understanding and overt motor behavior. Experimental Brain Research, 196, 403–412.

    PubMed  Article  Google Scholar 

  20. Daum, I., & Ackerman, H. (1994). Frontal-type memory impairment associated with thalamic damage. Internatonal Journal of Neuroscience, 75, 153–165.

    CAS  Article  Google Scholar 

  21. de Bie, R. M. A., de Haan, R. J., Nijssen, P. C. G., Rutgers, A. W. F., Beute, G. N., Bosch, D. A., et al. (1999). Unilateral pallidotomy in Parkinson’s disease: a randomised, single-blind, multicentre trial. Lancet, 354, 1665–1669.

    PubMed  Article  Google Scholar 

  22. Dogali, M., Fazzini, E., Kolodny, E., Eidelberg, D., Sterio, D., Devinsky, O., et al. (1995a). Stereotactic ventral pallidotomy for Parkinson’s disease. Neurology, 45, 753–761.

    CAS  PubMed  Article  Google Scholar 

  23. Dogali, M., Fazzini, E., Kolodny, E., Eidelberg, D., Sterio, D., Devinsky, O., et al. (1995b). Stereotactic ventral pallidotomy for Parkinson’s disease. Neurology, 45, 753–761.

    CAS  PubMed  Article  Google Scholar 

  24. Dogali, M., Sterio, D., Fazzini, E., Kolodny, E., Eidelberg, D., & Beric, A. (1996). Effects of posteroventral pallidotomy on Parkinson’s disease. Advances in Neurology, 69, 585–590.

    CAS  PubMed  Google Scholar 

  25. Eggert, G. H. (1977). Wernicke’s works in aphasia: a sourcebook and review (Vol. 1). The Hague, Netherlands: Mouton.

    Google Scholar 

  26. Elman, J. L., Bates, E. A., Johnson, M. H., Karmiloff-Smith, A., Parisi, D., & Plunkett, K. (1996). Rethinking Innateness. A Connectionist Perspective on Development. Cambridge, MA: MIT Press.

    Google Scholar 

  27. Felleman, D. J., & van Essen, D. C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex, 1, 1–47.

    CAS  PubMed  Article  Google Scholar 

  28. Fernandino, L., & Iacoboni, M. (2010). Are cortical motor maps based on body parts of coordinated actions? Implications for embodied semantics. Brain and Language, 112, 44–53.

    PubMed  Article  Google Scholar 

  29. Ferretti, T. R., McRae, K., & Hatherell, A. (2001). Integrating verbs, situation schemas, and thematic role concepts. Journal of Memory and Language, 44, 516–547.

    Article  Google Scholar 

  30. Fiore, V. G., Dolan, R. J., Strausfeld, N. J., & Hirth, F. (2015). Evolutionarily conserved mechanisms for the selection and maintenance of behavioral activity. Philosophoical Transactions of the Royal Society B, 370, 1–12.

    Google Scholar 

  31. Fiore, V. G., Sperati, V., Mannella, F., Mirolli, M., Gurney, K., Friston, K., et al. (2014). Keep focusing: striatal dopamine multiple functions resolved in a single mechanism tested in a simulated humanoid robot. Frontiers in Psychology, 21, 1–17.

    Google Scholar 

  32. Forde, E. M. E., & Humphreys, G. W. (1999). Category specific recognition impairments: a review of important case studies and influential theories. Aphasiology, 13, 169–193.

    Article  Google Scholar 

  33. Frak, V., Nazir, T. A., Goyette, M., Cohen, H., & Jeannerod, M. (2010). Grip force is part of the semantic representation of manual action verbs. PLoS ONE, 5(3), e9728.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  34. Fries, P. (2015). Rhythms for cognition: communication through coherence. Neuron, 88, 220–234.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Gasparini, M., Hufty, A. M., Masciarelli, G., Ottaviani, D., Angeloni, U., Lenzi, G. L., et al. (2008). Contribution of right hemisphere to visual imagery. A visual working memory impairment? Journal of the International Neuropsychological Society, 14, 902–911.

    PubMed  Article  Google Scholar 

  36. Georgopoulos, A. P., Kalaska, J. F., Caminiti, R., & Massey, J. T. (1982). On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. Journal of Neuroscience, 2, 1527–1537.

    CAS  PubMed  Article  Google Scholar 

  37. Gerfen, C. R., & Surmeier, D. J. (2011). Modulation of striatal projection systems by dopamine. Annual Review of Neuroscience, 34, 441–466.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. Grillner, S., & Robertson, B. (2016). The basal ganglia over 500 million years. Current Biology, 26, R1088–R1100.

    CAS  PubMed  Article  Google Scholar 

  39. Groh, A., Bokor, H., Mease, R. A., Plattner, V. M., Hangya, B., Stroh, A., et al. (2014). Convergence of cortical and sensory driver inputs on single thalamocortical cells. Cerebral Cortex, 24, 3167–3179.

    PubMed  Article  Google Scholar 

  40. Gross, R. E., Lombardi, W. J., Lang, A. E., Duff, J., Hutchison, W. D., Saint-Cyr, J. A., et al. (1999). Relationship of lesion location to clinical outcome following microeloectdrode-guided pallidotomy for Parkinson’s disease. Brain, 122, 405–416.

    PubMed  Article  Google Scholar 

  41. Haberly, L. B. (2001). Parallel-distributed processing in olfactory cortex: new insights from morphologivsl and physiological analysis of neuronal circuitry. Chemical Senses, 26, 551–576.

    CAS  PubMed  Article  Google Scholar 

  42. Halassa, M. M., & Sherman, S. M. (2019). Thalamocortical circuit motifs: a general framework. Neuron, 103, 762–770.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. Hayashi, R., Hashimoto, T., Tada, T., & Ikeda, S.-I. (2003). Effects of unilateral pallidotomy on voluntary movement, and simple and choice reaction times in Parkinson’s disease. Movement Disorders, 18, 515–523.

    PubMed  Article  Google Scholar 

  44. Hirsch, J. A., Wang, X., Sommer, F. T., & Martinez, L. M. (2015). How inhibitory circuits in the thalamus serve vision. Annual Review of Neuroscience, 38, 309–329.

    CAS  PubMed  Article  Google Scholar 

  45. Homman-Ludiye, J., & Bourne, J. A. (2019). The medial pulvinar: function, origin and association with neurodevelopmental disorders. Journal of Anatomy, 235, 507–520.

    PubMed  Article  Google Scholar 

  46. Humphries, M. D., Obeso, J. A., & Dreyer, J. K. (2018). Insights into Parkinson’s disease from computational models of basal ganglia function. Journal of Neurology, Neurosurgery, and Psychiatry, 89, 1181–1188.

    PubMed  PubMed Central  Article  Google Scholar 

  47. Humphries, M. D., Stewart, J. T., & Gurney, K. (2006). A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. Journal of Neuroscience, 26, 12921–12942.

    CAS  PubMed  Article  Google Scholar 

  48. Jaramillo, J., Mejias, J. F., & Wang, X.-J. (2019). Engagement of pulvino-cortical feedforward and feedback pathways in cognitive computaitions. Neuron, 101, 321–336.

    CAS  PubMed  Article  Google Scholar 

  49. Johansen-Berg, H., Behrens, T. E. J., Sillery, E. L., Ciccarelli, O., Thompson, A. J., Smith, S. M., et al. (2005). Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cerebral Cortex, 15, 31–39.

    PubMed  Article  Google Scholar 

  50. Jones, E. G. (2001). The thalamic matrix and thalamocortical synchrony. Trends in Neuroscience, 24, 596–601.

    Google Scholar 

  51. Jones, E. G. (2002). thalamic circuitry and thalamocortical synchrony. Philosophical Transactions of the Royal Society B, 357, 1659–1673.

    Article  Google Scholar 

  52. Kahneman, D. (2011). Thinking, Fast and Slow. New York: Farrar, Straus and Giroux.

    Google Scholar 

  53. Kemmerer, D., Gonzalez Castillo, J., Talavage, T., Patterson, S., & Wiley, C. (2008). Neuronanatomical distribution of five semantic components of verbs: evidence from fMRI. Brain and Language, 107, 16–43.

    PubMed  Article  Google Scholar 

  54. Kemmerer, D., & Gonzalez-Castillo, J. (2010). The two-level theory of verb meaning: an approach to integrating the semantics of action with the mirror neuron system. Brain and Language, 112, 54–76.

    PubMed  Article  Google Scholar 

  55. Kishore, A., Turnbull, I. M., Snow, B. J., de la Fuente-Ferrnandez, R., Schulzer, M., Mak, E., et al. (1997). Efficacy, stability and predictors of outcome of pallidotomy for Parkinson’s disease. Six-month follow-up with additional 1-year observations. Brain, 120, 729–737.

    PubMed  Article  Google Scholar 

  56. Kumaran, D., Hassabis, D., & McClelland, J. L. (2016). What learning systems do intelligent agents need? Complementary learning systems theory updated. Trends in Cognitive Science, 20, 512–534.

    Article  Google Scholar 

  57. Kuramoto, E., S., P., Furuta, T., Tanaka, Y. R., Iwai, H., Yamanaka, A., , et al. (2017). Individual mediodorsal thalamic neurons poject to multiple areas of the rat prefrontal cortex: a single neuron-tracing study using virus vectors. Journal of Comparative Neurology, 525, 166–185.

    Article  Google Scholar 

  58. Lang, A. E., Lozano, A. M., Montgomery, E., Duff, J., Tasker, R., & Hutchison, W. (1997). Posteroventral medial pallidotomy in advanced Parkinson’s disease. New England Journal of Medicine, 337, 1036–1042.

    CAS  Article  Google Scholar 

  59. Lebedev, M. A., & Nicolelis, M. A. (2017). Brain-machine interfaces: from basic science to neuroprostheses and neurorehabilitation. Physiological Reviews, 97, 767–837.

    PubMed  Article  Google Scholar 

  60. Lissauer, H. (1988). Ein fall von seelenblindheit nebst einem beitrag sur theorie derselven. Cognitive Neuropsychology, 5, 157–192.

    Article  Google Scholar 

  61. Malekmohammadi, M., Elias, W. J., & Pouratian, N. (2014). Human thalamus regulates cortical activity via spatially specific and structurally constrained phase-amplitude coupling. Cerebral Cortex, 25, 1618–1628.

    PubMed  Article  Google Scholar 

  62. Mannella, F., & Baldassarre, G. (2015). Selection of cortical dynamics for motor behavior by the basal ganglia. Biological Cybernetics, 109, 575–595.

    PubMed  PubMed Central  Article  Google Scholar 

  63. Marshall, J., Chiat, S., Robson, J., & Pring, T. (1996). Calling a salad a federation: an investigation of semantic jargon. Part 2 — verbs. Journal of Neurolinguistics, 4, 251–260.

    Article  Google Scholar 

  64. McAlonan, K., Cavanaugh, J., & Wurtz, R. H. (2008). Guarding the gateway to cortex with attention in visual thalamus. Nature, 456, 391–394.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. McClelland, J. L., Mirman, D., Bolger, D. J., & Khaitan, P. (2014). Interactive activation and mutual constraint satisfaction in perception and cognition. Cognitive Science, 38, 1139–1189.

    PubMed  Article  Google Scholar 

  66. McClelland, J. L., Rumelhart, D. E., & Hinton, G. E. (1986a). The appeal of parallel distributed processing. In D. E. Rumelhart, J. L. McClelland, & the PDP Processing Group (Eds.), Parallel Distributed Processing (Vol. 1, pp. 3–44). Cambridge, MA: MIT Press.

  67. McClelland, J. L., Rumelhart, D. E., & PDP Research Group. (1986). Parallel Distributed Processing. Cambridge, MA: MIT Press.

    Google Scholar 

  68. McCormick, D. A., & Feeser, H. R. (1990). Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience, 39, 103–113.

    CAS  PubMed  Article  Google Scholar 

  69. McRae, K., Hare, M., Elman, J. L., & Ferretti, T. R. (2005). A basis for generating expectancies for verbs from nouns. Memory and Cognition, 33, 1174–1184.

    PubMed  Article  Google Scholar 

  70. Mennemeier, M., Fennell, E., Valenstein, E., & Heilman, K. M. (1992). Contributions of the left intralaminar and medial thalamic nuclei to memory. Archives of Neurology, 49, 1050–1058.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. Middleton, F. A., & Strick, P. L. (1997). New concepts about the organization of the basal ganglia output. Advances in Neurology, 74, 57–68.

    CAS  PubMed  Google Scholar 

  72. Mo, C., & Sherman, S. M. (2019). A sensorimotor pathway via higher-order thalamus. Journal of Neuroscience, 39, 692–704.

    CAS  PubMed  Article  Google Scholar 

  73. Nadeau, S. E. (2012). The Neural Architecture of Grammar. Cambridge, MA: MIT Press.

    Google Scholar 

  74. Nadeau, S. E. (2014). Attractor basins: a neural basis for the conformation of knowledge. In A. Chatterjee & H. B. Coslett (Eds.), The Roots of Cognitive Neuroscience (pp. 305–333). Oxford: Oxford University Press.

    Google Scholar 

  75. Nadeau, S. E. (2015). Neuroplastic mechanisms of language recovery after stroke. In J. I. Tracy, B. M. Hampstead, & K. Sathian (Eds.), Cognitive Plasticity in Neurologic Disorders (pp. 61–84). New York: Oxford University Press.

    Google Scholar 

  76. Nadeau, S. E. (2019). Bilingual aphasia: explanations in population encoding. J Neurolinguistics, 49, 117–143.

    Article  Google Scholar 

  77. Nadeau, S. E. (2020). Neural population dynamics and cognitive function. Frontiers in Human Neuroscience, 14(50). https://doi.org/10.3389/fnhum.2020.00050

  78. Nadeau, S. E., & Crosson, B. (1997). Subcortical aphasia. Brain and Language, 58(355–402), 436–458.

    Article  Google Scholar 

  79. O’Keefe, J., & Nadel, L. (1979). The hippocampus as a cognitive map. Behavioral Brain Sciences, 2, 487–533.

    Article  Google Scholar 

  80. Ocana, F. M., Suryanarayana, S. M., Robertson, B., & Grillner, S. (2015). The lamprey pallium provides a blueprint of the mammalian motor projections from the cortex. Current Biology, 25, 413–423.

    CAS  PubMed  Article  Google Scholar 

  81. Percheron, G., Yelnik, J., & François, C. (1984). A Golgi analysis of the primate globus pallidus. III. Spatial organization of the striato-pallidal complex. Journal of Comparative Neurology, 227, 214–227.

    CAS  Article  Google Scholar 

  82. Pergola, G., Bellebaum, C., Gehlhaar, B., Koch, B., Schwarz, M., Daum, I., et al. (2013). The involvement of the thalamus in semantic retrieval: a clinical group study. Journal of Cognitive Neuroscience, 25, 872–886.

    PubMed  Article  PubMed Central  Google Scholar 

  83. Pinault, D. (2004). The thalamic reticular nucleus: structure, function, and concerpt. Brain Research Reviews, 46, 1–31.

    PubMed  Article  PubMed Central  Google Scholar 

  84. Pirini, M., Rocchi, L., Sensi, M., & Chiari, L. (2009). A computational modelling approach to investigate different targets in deep brain stimulation for Parkinson’s disease. Journal of Computational Neuroscience, 26, 91.

    PubMed  Article  PubMed Central  Google Scholar 

  85. Plaut, D. C., McClelland, J. L., Seidenberg, M. S., & Patterson, K. (1996). Understanding normal and impaired word reading: computational principles in quasi-regular domains. Psychological Review, 103, 56–115.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  86. Plaut, D. C., & Vande Velde, A. K. (2017). Statistical learning of parts and wholes: a neural network approach. Journal of Experimentsl Psychology: General, 146, 318–336.

    Article  Google Scholar 

  87. Plotkin, J. L., & Goldberg, J. A. (2019). Thinking outside the box (and arrow): current themes in striatal dysfunction in movement disorders. Neuroscientist, 25, 359–379.

    PubMed  Article  PubMed Central  Google Scholar 

  88. Pulvermüller, F. (2010). Brain embodiment of syntax and grammar: discrete combinatorial mechanisms spelt out in neural circuits. Brain and Language, 112, 167–179.

    PubMed  Article  Google Scholar 

  89. Raymer, A. M., Moberg, P., Crosson, B., Nadeau, S., & Gonzalez Rothi, L. J. (1997). Lexical-semantic deficits in two patients with dominant thalamic infarction. Neuropsychologia, 35, 211–219.

    CAS  PubMed  Article  Google Scholar 

  90. Redgrave, P., Prescott, T. J., & Gurney, K. (1999). The basal ganglia: a vertebrate solution to the selection problem. Neuroscience, 89, 1009–1023.

    CAS  PubMed  Article  Google Scholar 

  91. Rockland, K. S. (2019). Corticothalamic axon morphologies and network architecture. European Journal of Neuroscience, 49, 969–977.

    Article  Google Scholar 

  92. Rogers, T. T., & McClelland, J. L. (2014). Parallel distributed processing at 25: further explorations in the microstructure of cognition. Cognitive Science, 38, 1025–1077.

    Article  Google Scholar 

  93. Rolls, E. T. (2016). Cerebral Cortex: Principles of Operation. Oxford: Oxford University Press.

    Google Scholar 

  94. Rolls, E. T., & Deco, G. (2002). Computational Neuroscience of Vision. Oxford: Oxford University Press.

    Google Scholar 

  95. Rolls, E. T., & Treves, A. (1998). Neural networks and brain function. New York: Oxford University Press.

    Google Scholar 

  96. Romanski, L. M., Giguere, M., Bates, J. F., & Goldman-Rakic, P. S. (1997). Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology, 379, 313–332.

    CAS  Article  Google Scholar 

  97. Rovó, Z., Ulbert, I., & Acsády, L. (2012). Drivers of the primate thalamus. Journal of Neuroscience, 32, 17894–17908.

    PubMed  Article  CAS  Google Scholar 

  98. Rubin, J. E. (2017). Compuetational models of basal ganglia dysfunction: the dynamics is in the details. Current Opinion in Neurology, 46, 127–135.

    CAS  Article  Google Scholar 

  99. Saalmann, Y. B., & Kastner, S. (2011). Cognitive and perceptual functions of the visual thalamus. Neuron, 71, 209–223.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  100. Saalmann, Y. B., Pinsk, M. A., Wang, L., Li, X., & Kastner, S. (2012). The pulvinar regulates information transmission between cortical areas based on attention demands. Science, 337, 753–756.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  101. Sadikot, A. F., & Rymer, V. V. (2009). The primate centromedian-parafascicular complex: anatomical organization with a note on neuromodulation. Brain Research Bulletin, 78, 122–130.

    PubMed  Article  Google Scholar 

  102. Samii, A., Turnbull, I. M., Kishore, A., Schulzer, M., Mak, E., Yardley, S., et al. (1999). Reassessment of unilateral pallidotomy in Parkinson’s disease. A 2-year follow-up study. Brain, 122, 417–425.

    PubMed  Article  Google Scholar 

  103. Scheibel, M. E., & Scheibel, A. B. (1967). Structural organization of nonspecific thalamic nuclei and their projection toward cortex. Brain Research, 6, 60–94.

    CAS  PubMed  Article  Google Scholar 

  104. Scheibel, M. E., & Scheibel, A. B. (1972). Specialized organizational patterns within the nucleus reticularis thalami of the cat. Experimental Neurology, 34, 316–322.

    CAS  PubMed  Article  Google Scholar 

  105. Seidenberg, M. S., & McClelland, J. L. (1989). A distributed, developmental model of word recognition and naming. Psychogy Review, 96, 523–568.

    CAS  Article  Google Scholar 

  106. Sherman, S. M. (2016). Thalamus plays a central role in ongoing cortical functioning. Nature Neuroscience, 19, 533–541.

    CAS  PubMed  Article  Google Scholar 

  107. Skinner, J. E., & Yingling, C. D. (1977). Central gating mechanisms that regulate event-related potentials and behavior. In J. E. Desmedt (Ed.), Attention, voluntary contraction and event-related cerebral potentials (pp. 30–69). Basel: Karger.

    Google Scholar 

  108. Speedie, L. J., & Heilman, K. M. (1982). Amnestic disturbance following infarction of thr left dorsomedial nucleus of the thalamus. Neuropsychologia, 20, 597–604.

    CAS  PubMed  Article  Google Scholar 

  109. Stephenson-Jones, M., Samuelsson, E., Ericsson, J., Robertson, B., & Grillner, S. (2011). Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Current Biology, 21, 1081–1091.

    CAS  PubMed  Article  Google Scholar 

  110. Steriade, M. (2006). Grouping of brain rhythms in corticothalamic systems. Neuroscience, 137, 1087–1106.

    CAS  PubMed  Article  Google Scholar 

  111. Steriade, M., Jones, E. G., & Llinas, R. R. (1990). Thalamic oscillations and signaling. New York: John Wiley and Sons.

    Google Scholar 

  112. Steriade, M., & Llinás, R. R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews, 68, 649–742.

    CAS  PubMed  Article  Google Scholar 

  113. Stitt, I., Zhou, Z. C., Radtke-Schuller, S., & Frölich, F. (2018). Arousal dependent modulation of thalamo-cortical functional interaction. Nature Communations, 9(2455), 1–13.

    CAS  Google Scholar 

  114. Strausfeld, N. J., & Hirth, F. (2013a). Deep homology of arthropod central complex and vertebrate basal ganglia. Science, 340, 157–161.

    CAS  PubMed  Article  Google Scholar 

  115. Strausfeld, N. J., & Hirth, F. (2013b). Deep homology ofarthropod central complex and vertebrate basal ganglia. Science, 340, 157–161.

    CAS  PubMed  Article  Google Scholar 

  116. Tang, H., Schrimpf, M., Lotter, W., Moerman, C., Paredes, A., & Caro, J. O. (2018). Recurrent computations for visual pattern completion. Proceedings of the National Academy of Sciences USA, 115, 8835–8840.

    CAS  Article  Google Scholar 

  117. Taylor, L. J., & Zwaan, R. A. (2008). Motor resonance and linguistic focus. Quarterly Journal of Experimental Psychology, 61, 896–904.

    Article  Google Scholar 

  118. Theyel, B. B., Llano, D. A., & Sherman, S. M. (2010). the corticothalamocortical circuit drives higher-order cortex in the mouse. Nature Neuroscience, 13, 84–88.

    CAS  PubMed  Article  Google Scholar 

  119. Usrey, W. M., & Sherman, S. M. (2017). Corticofugal circuits: communication lines from the cortex to the rest of the brain. Journal of Comparative Neurology, 527, 640–650.

    Article  Google Scholar 

  120. Van der Werf, Y. D., Weerts, J. G. E., Jolles, J., Witter, M. P., Lindeboom, J., & Scheltens, P. (1999). Neuropsychological correlates of a right unilateral lacunar thalamic infarction. Journal of Neurology, Neurosurgery, and Psychiatry, 66, 36–42.

    PubMed Central  Article  Google Scholar 

  121. Vitek, J. L., Bakay, R. A. E., & DeLong, M. R. (1997). Microelectrode-guided pallidotomy for medically intractable Parkinson’s disease. Advances in Neurology, 74, 183–198.

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Vitek, J. L., Bakay, R. A. E., Freeman, A., Evatt, M., Greene, J., McDonald, W., et al. (2003). Randomized trial of pallidotomy versus medical therapy for Parkinson’s disease. Annals of Neurology, 53, 558–569.

    PubMed  Article  PubMed Central  Google Scholar 

  123. von Monakow, C. (1914). Die Lokalisation im Grosshirn. Wiesbaden: Bergmann.

    Google Scholar 

  124. Wang, S., Bickford, M. E., Van Horn, S. C., Erisir, A., Goodwin, D. W., & Sherman, S. M. (2001). Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat. Journal of Comparative Neurology, 440, 321–334.

  125. Wang, X., Wei, Y., Vaingankar, V., Wang, Q., Koepsell, K., Sommer, F. T., et al. (2007). Feedforward excitation and inhibition evoke dual modes of firing in the cat’s visual thalamus during naturalistic viewing. Neuron, 55, 465–478.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. Warrington, E. K., & Shallice, T. (1984). Category specific semantic impairments. Brain, 107, 829–854.

    PubMed  Article  Google Scholar 

  127. Wilson, C. J. (2007). GABAergic inhibition in the neostriatum. Progress in Brain Research, 160, 91–110.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  128. Wimmer, R. D., Schmitt, L. I., Davidson, T. J., Nakajima, M., & D’eisseroth, K., & Halassa, M. M. . (2015). Thalamic control of sensory selection in divided attention. Nature, 526, 705. https://doi.org/10.1038/nature15398

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  129. Yelnik, J. (2002). Functional anatomy of the basal ganglia. Movement Disorders, 17, S15–S21.

    PubMed  Article  Google Scholar 

  130. Zajzon, B., & Morales-Gregorio, A. (2019). Trans-thalamic pathways: strong candidates for supporting communication between functional distinct cortical areas. Journal of Neuroscience, 39, 7034–7036.

    CAS  PubMed  Article  Google Scholar 

  131. Zhang, K., Ginzburg, I., McNaughton, B. L., & Sejnowski, T. J. (1998). Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. Journal of. Neurophysiology, 79, 1017–1044.

    CAS  PubMed  Article  Google Scholar 

  132. Zhang, K., & Sejnowski, T. J. (1999). Neuronal tuning: to sharpen or broaden? Neural Computation, 11, 75–84.

    CAS  PubMed  Article  Google Scholar 

  133. Zhou, H., Schafer, R. J., & Desimone, R. (2016). Pulvinar-cortex interactions in vision and attention. Neuron, 89, 209–220.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  134. Zikopoulos, B., & Barbas, H. (2006). Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. Journal of Neuroscience, 26, 7348–7361.

    CAS  PubMed  Article  Google Scholar 

Download references

Funding

This work was supported by resources provided by the North Florida/South Georgia Veterans Health System, Gainesville, FL. It was not supported by a specific grant from funding agencies in the public, commercial, or not-for-profit sectors. I am very grateful to John Richardson for creation of many of the figures. The contents of this manuscript do not represent the views of the U.S. Department of Veterans Affairs, the United States Government, or the University of Florida.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Stephen E. Nadeau.

Ethics declarations

Conflicts of Interest

The author has no conflicts of interest bearing on this manuscript.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nadeau, S.E. Basal Ganglia and Thalamic Contributions to Language Function: Insights from A Parallel Distributed Processing Perspective. Neuropsychol Rev (2021). https://doi.org/10.1007/s11065-020-09466-0

Download citation

Keywords

  • Parallel distributed processing
  • Basal ganglia
  • Thalamus
  • Language