Abstract
Brief maneuvering of the literature as to the various roles attributed to the basal ganglia corticostriatal circuits in a variety of cognitive processes such as working memory, selective attention, and category learning has inspired us to investigate the interplay of the two major basal ganglia open-recurrent loops, namely, visual and executive loops specifically the possible involvement of their overlap in conditional learning. We propose that the interaction of the visual and executive loops reflected through their cortical overlap in the dorsolateral prefrontal cortex (DL-PFC), lateral orbitofrontal cortex (LO-PFC), and presupplementary motor area (SMA) plays an instrumental role preliminary first in forming associations between a series of correct responses following similar stimuli and then in shifting, abstracting, and generalizing conditioned responses. The premotor and supplementary motor areas have been shown essential to producing a sequence of movements while the SMA is engaged in monitoring complex movements. In light of the recent studies, we will suggest that the interaction of visual and executive loops could strengthen or weaken learned associations following different reward values. Furthermore, we speculate that the overlap of the visual and executive loops can account for the switching between the associative vs. rule-based category learning systems.
Acknowledgment
I shall thank Prof. Fred Hamker from Chemnitz University of Technology who provided insight and expertise that significantly assisted this work, although he may not agree with all of the interpretations/conclusions suggested in this paper.
Author contribution: The author has accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Conflict of interest statement: The author declares no conflicts of interest regarding this article.
References
Alexander, G.E., Delong, M.R., and Strick, P. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci 9: 357–81. https://doi.org/10.1146/annurev.ne.09.030186.002041.10.1146/annurev.ne.09.030186.002041Search in Google Scholar PubMed
Antzoulatos, E.G. and Miller, E.K. (2011). Differences between neural activity in prefrontal cortex and striatum during learning of novel abstract categories. Neuron 71, 243–249. https://doi.org/10.1016/j.neuron.2011.05.040.10.1016/j.neuron.2011.05.040Search in Google Scholar PubMed PubMed Central
Aoki, S., Smith, J.B., Li, H., Yan, X., Igarashi, M., Coulon, P., Wickens, J.R., Ruigrok, T.J., and Jin, X. (2019). An open cortico-basal ganglia loop allows limbic control over motor output via the nigrothalamic pathway. Elife 8. https://doi.org/10.7554/elife.49995.10.7554/eLife.49995.021Search in Google Scholar
Baladron, J. and Hamker, F.H. (2020). Habit learning in hierarchical cortex - basal ganglia loops. Eur. J. Neurosci. https://doi.org/10.1111/ejn.14730.10.1111/ejn.14730Search in Google Scholar PubMed
Bédard, P. and Sanes, J.N. (2009). On a basal ganglia role in learning and rehearsing visual?motor associations. Neuroimage 47: 1701–1710. https://doi.org/10.1016/j.neuroimage.2009.03.050.10.1016/j.neuroimage.2009.03.050Search in Google Scholar PubMed PubMed Central
Cantwell, G., Riesenhuber, M., Roeder, J.L., and Ashby, F.G. (2017). Perceptual category learning and visual processing: an exercise in computational cognitive neuroscience. Neural Network. 89: 31–38. https://doi.org/10.1016/j.neunet.2017.02.010.10.1016/j.neunet.2017.02.010Search in Google Scholar PubMed PubMed Central
Cebrián, C., Parent, A., and Prensa, L. (2005). Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat. J. Comp. Neurol 492: 349–369. https://doi.org/10.1002/cne.20741.10.1002/cne.20741Search in Google Scholar PubMed
Chatham, C.H., Herd, S.A., Brant, A.M., Hazy, T.E., Miyake, A., O’Reilly, R., and Friedman, N.P. (2011). From an executive network to executive control: a computational model of the n-back task. J. Cognit. Neurosci. 23: 3598–3619. https://doi.org/10.1162/jocn_a_00047.10.1162/jocn_a_00047Search in Google Scholar PubMed PubMed Central
Choi, E.Y., Yeo, B.T.T., and Buckner, R.L. (2012). The organization of the human striatum estimated by intrinsic functional connectivity. J. Neurophysiol. 108 8: 2242–63. https://doi.org/10.1152/jn.00270.2012.10.1152/jn.00270.2012Search in Google Scholar PubMed PubMed Central
DeLong, M. and Wichmann, T. (2010). Changing views of basal ganglia circuits and circuit disorders. Clin. EEG Neurosci. 41: 61–67. https://doi.org/10.1177/155005941004100204.10.1177/155005941004100204Search in Google Scholar PubMed PubMed Central
Draganski, B., Kherif, F., Klöppel, S., Cook, P.A., Alexander, D.C., Parker, G.J.M., Deichmann, R., Ashburner, J., and Frackowiak, R.S. (2008). Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J. Neurosci. Res 28: 7143–52. https://doi.org/10.1523/jneurosci.1486-08.2008.10.1523/JNEUROSCI.1486-08.2008Search in Google Scholar PubMed PubMed Central
Eisinger, R.S., Cernera, S., Gittis, A.H., Gunduz, A., and Okun, M.S. (2019). A review of basal ganglia circuits and physiology: application to deep brain stimulation. Park. Relat. Disord. 59: 9–20. https://doi.org/10.1016/j.parkreldis.2019.01.009.10.1016/j.parkreldis.2019.01.009Search in Google Scholar PubMed PubMed Central
Frank, M.J. (2006). Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Network.: The Off. J. Int. Neural Net. Soc. 19: 1120–36. https://doi.org/10.1016/j.neunet.2006.03.006.10.1016/j.neunet.2006.03.006Search in Google Scholar PubMed
Gallay, M.N., Jeanmonod, D., Liu, J., and Morel, A. (2008). Human pallidothalamic and cerebellothalamic tracts: anatomical basis for functional stereotactic neurosurgery. Brain Struct. Funct. 212: 443–463. https://doi.org/10.1007/s00429-007-0170-0.10.1007/s00429-007-0170-0Search in Google Scholar PubMed PubMed Central
Guthrie, M., Leblois, A., Garenne, A., and Boraud, T. (2013). Interaction between cognitive and motor cortico-basal ganglia loops during decision making: a computational study. J. Neurophysiol. 109: 3025–40. https://doi.org/10.1152/jn.00026.2013.10.1152/jn.00026.2013Search in Google Scholar PubMed
Hadj-Bouziane, F., Benatru, I., Brovelli, A., Klinger, H., Thobois, S., Broussolle, E., Boussaoud, D., and Meunier, M. (2013). Advanced Parkinson’s disease effect on goal-directed and habitual processes involved in visuomotor associative learning. Front. Hum. Neurosci. 6: 351. https://doi.org/10.3389/fnhum.2012.00351.10.3389/fnhum.2012.00351Search in Google Scholar PubMed PubMed Central
Haruno, M. and Kawato, M. (2006). Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J. Neurophysiol. 95: 948–59. https://doi.org/10.1152/jn.00382.2005.10.1152/jn.00382.2005Search in Google Scholar PubMed
Helie, S., Chakravarthy, S., and Moustafa, A.A. (2013). Exploring the cognitive and motor functions of the basal ganglia: an integrative review of computational cognitive neuroscience models. Front. Comput. Neurosci. 7: 174. https://doi.org/10.3389/fncom.2013.00174.10.3389/fncom.2013.00174Search in Google Scholar PubMed PubMed Central
Hikosaka, O., Takikawa, Y., and Kawagoe, R. (2000). Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80: 953–978. https://doi.org/10.1152/physrev.2000.80.3.953.10.1152/physrev.2000.80.3.953Search in Google Scholar PubMed
Hoshi, E. (2013). Cortico-basal ganglia networks subserving goal-directed behavior mediated by conditional visuo-goal association. Front. Neural Circ. 7: 158. https://doi.org/10.3389/fncir.2013.00158.10.3389/fncir.2013.00158Search in Google Scholar PubMed PubMed Central
Humphries, M.D., Stewart, R.D., and Gurney, K.N. (2006). A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci. Res 26: 12921–42. https://doi.org/10.1523/jneurosci.3486-06.2006.10.1523/JNEUROSCI.3486-06.2006Search in Google Scholar
Lawrence, A.D., Sahakian, B.J., and Robbins, T.W. (1998). Cognitive functions and corticostriatal circuits: insights from huntington’s disease. Trends Cognit. Sci. 2: 379–388. https://doi.org/10.1016/s1364-6613(98)01231-5.10.1016/S1364-6613(98)01231-5Search in Google Scholar
Leh, S.E., Ptito, A., Chakravarty, M.M., and Strafella, A.P. (2007). Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study. Neurosci. Lett 419: 113–118. https://doi.org/10.1016/j.neulet.2007.04.049.10.1016/j.neulet.2007.04.049Search in Google Scholar
Leisman, G., Braun-Benjamin, O., and Melillo, R. (2014). Cognitive-motor interactions of the basal ganglia in development. Front. Syst. Neurosci. 8. https://doi.org/10.3389/fnsys.2014.00016.10.3389/fnsys.2014.00016Search in Google Scholar
Leung, H.-C.E., Gore, J.C., and Goldman-Rakic, P.S. (2002). Sustained mnemonic response in the human middle frontal gyrus during on-line storage of spatial memoranda. J. Cognit. Neurosci. 14: 659–671. https://doi.org/10.1162/08989290260045882.10.1162/08989290260045882Search in Google Scholar
Lopez-Paniagua, D. and Seger, C.A. (2011). Interactions within and between corticostriatal loops during component processes of category learning. J. Cognit. Neurosci. 23: 3068–3083. https://doi.org/10.1162/jocn_a_00008.10.1162/jocn_a_00008Search in Google Scholar
Love, B.C. and Tomlinson, M. (2010). Mechanistic models of associative and rule-based category learning: the making of human concepts. Oxford University Press, United Kingdom, pp. 53–74.Search in Google Scholar
Middleton, F.A. and Strick, P. (1996). The temporal lobe is a target of output from the basal ganglia. Proc. Natl. Acad. Sci. U.S.A. 93, 8683–7. https://doi.org/10.1073/pnas.93.16.8683.10.1073/pnas.93.16.8683Search in Google Scholar
Nasser, H.M., Calu, D.J., Schoenbaum, G., and Sharpe, M.J. (2017). The dopamine prediction error: contributions to associative models of reward learning. Front. Psychol. 8. https://doi.org/10.3389/fpsyg.2017.00244.10.3389/fpsyg.2017.00244Search in Google Scholar
Picard, N. and Strick, P.L. (1996). Motor areas of the medial wall: a review of their location and functional activation. Cerebr. Cortex 6: 342–353. https://doi.org/10.1093/cercor/6.3.342.10.1093/cercor/6.3.342Search in Google Scholar
Puri, B.K. and Hall, A.D. (2014). Revision notes in psychiatry, 3rd ed. Boca Raton, Florida: CRC Press.Search in Google Scholar
Redgrave, P., Prescott, T.J., and Gurney, K. (1999). The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89: 1009–1023. https://doi.org/10.1016/s0306-4522(98)00319-4.10.1016/S0306-4522(98)00319-4Search in Google Scholar
Robinson, J.L., Laird, A.R., Glahn, D.C., Blangero, J., Sanghera, M.K., Pessoa, L., Fox, P.M., Uecker, A., Friehs, G., Young, K.A., et al. (2012). The functional connectivity of the human caudate: an application of meta-analytic connectivity modeling with behavioral filtering. Neuroimage 60: 117–129. https://doi.org/10.1016/j.neuroimage.2011.12.010.10.1016/j.neuroimage.2011.12.010Search in Google Scholar PubMed PubMed Central
Saint-Cyr, J.A., Ungerleider, L.G., and Desimone, R. (1990). Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. J. Comp. Neurol 298: 129–56. https://doi.org/10.1002/cne.902980202.10.1002/cne.902980202Search in Google Scholar PubMed
Schroll, H., Vitay, J., and Hamker, F.H. (2012). Working memory and response selection: a computational account of interactions among cortico-basalganglio-thalamic loops. Neural Network. 26: 59–74. https://doi.org/10.1016/j.neunet.2011.10.008.10.1016/j.neunet.2011.10.008Search in Google Scholar PubMed
Seger, C.A. (2006). The basal ganglia in human learning. Neuroscientist 12: 285–290. https://doi.org/10.1177/1073858405285632.10.1177/1073858405285632Search in Google Scholar PubMed
Seger, C.A. (2008). How do the basal ganglia contribute to categorization? their roles in generalization, response selection, and learning via feedback. Neurosci. Biobehav. Rev. 32: 265–278. https://doi.org/10.1016/j.neubiorev.2007.07.010.10.1016/j.neubiorev.2007.07.010Search in Google Scholar PubMed PubMed Central
Seger, C.A. and Cincotta, C.M. (2005). The roles of the caudate nucleus in human classification learning. J. Neurosci. 25: 2941–2951. https://doi.org/10.1523/jneurosci.3401-04.2005.10.1523/JNEUROSCI.3401-04.2005Search in Google Scholar PubMed PubMed Central
Seger, C.A. and Miller, E.K. (2010). Category learning in the brain. Annu. Rev. Neurosci 33: 203–19. https://doi.org/10.1146/annurev.neuro.051508.135546.10.1146/annurev.neuro.051508.135546Search in Google Scholar PubMed PubMed Central
Shires, J.A., Joshi, S., and Basso, M.A. (2010). Shedding new light on the role of the basal ganglia-superior colliculus pathway in eye movements. Curr. Opin. Neurobiol. 20: 717–725. https://doi.org/10.1016/j.conb.2010.08.008.10.1016/j.conb.2010.08.008Search in Google Scholar PubMed PubMed Central
Sitaram, R., Ros, T., Stoeckel, L., Haller, S., Scharnowski, F., Lewis-Peacock, J.A., Weiskopf, N., Blefari, M.L., Rana, M., Oblak, E., et al. (2017). Closed-loop brain training: the science of neurofeedback. Nat. Rev. Neurosci. 18: 86–100. https://doi.org/10.1038/nrn.2016.164.10.1038/nrn.2016.164Search in Google Scholar PubMed
Smith, J.G. and Mcdowall, J. (2011). Dissociating sequence learning performance in Parkinson’s disease: visuomotor sequence acquisition and pattern judgment on a serial reaction time task. Acta Neurobiol. Exp. 71: 359–380, http://doi.org/10.1037/t10132-000.10.1037/t10132-000Search in Google Scholar
Toni, I., Rowe, J., Stephan, K., and Passingham, R. (2002). Changes of cortico-striatal effective connectivity during visuomotor learning. Cerebr. Cortex 12: 1040–7. https://doi.org/10.1093/cercor/12.10.1040.10.1093/cercor/12.10.1040Search in Google Scholar
Trapp, S., Schroll, H., and Hamker, F.H. (2012). Open and closed loops: a computational approach to attention and consciousness. Adv. Cognit. Psychol. 8: 1. https://doi.org/10.5709/acp-0096-y.10.5709/acp-0096-ySearch in Google Scholar
Vanduffel, W. and Arsenault, J.T. (2016). Should i stay or should i go? Neuron 91: 207–210. https://doi.org/10.1016/j.neuron.2016.07.012.10.1016/j.neuron.2016.07.012Search in Google Scholar
Verstynen, T.D., Badre, D., Jarbo, K., and Schneider, W. (2012). Microstructural organizational patterns in the human corticostriatal system. J. Neurophysiol. 107: 2984–95. https://doi.org/10.1152/jn.00995.2011.10.1152/jn.00995.2011Search in Google Scholar
Webster, M., Ungerleider, L., and Bachevalier, J. (1991). Connections of inferior temporal areas te and teo with medial temporal-lobe structures in infant and adult monkeys. J. Neurosci. 11: 1095–1116. https://doi.org/10.1523/jneurosci.11-04-01095.1991.10.1523/JNEUROSCI.11-04-01095.1991Search in Google Scholar
Webster, M.J., Bachevalier, J., and Ungerleider, L.G. (1995). Transient subcortical connections of inferior temporal areas te and teo in infant macaque monkeys. J. Comp. Neurol 352: 213–26. https://doi.org/10.1002/cne.903520205.10.1002/cne.903520205Search in Google Scholar
Wei, W., Rubin, J.E., and Wang, X.-J. (2015). Role of the indirect pathway of the basal ganglia in perceptual decision making. J. Neurosci. 35: 4052–4064. https://doi.org/10.1523/jneurosci.3611-14.2015.10.1523/JNEUROSCI.3611-14.2015Search in Google Scholar
Wolfensteller, U. and Ruge, H. (2012). Frontostriatal mechanisms in instruction-based learning as a hallmark of flexible goal-directed behavior. Front. Psychol. 3. https://doi.org/10.3389/fpsyg.2012.00192.10.3389/fpsyg.2012.00192Search in Google Scholar
Yamamoto, S., Monosov, I.E., Yasuda, M., and Hikosaka, O. (2012). What and where information in the caudate tail guides saccades to visual objects. J. Neurosci. Res 32: 11005–16. https://doi.org/10.1523/jneurosci.0828-12.2012.10.1523/JNEUROSCI.0828-12.2012Search in Google Scholar
Yeterian, E.H. and Hoesen, G.W.V. (1978). Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res. 139: 43–63. https://doi.org/10.1016/0006-8993(78)90059-8.10.1016/0006-8993(78)90059-8Search in Google Scholar
Yeterian, E.H. and Pandya, D.N. (1995). Corticostriatal connections of extrastriate visual areas in rhesus monkeys. J. Comp. Neurol 352: 436–57. https://doi.org/10.1002/cne.903520309.10.1002/cne.903520309Search in Google Scholar PubMed
© 2020 Walter de Gruyter GmbH, Berlin/Boston
