Skip to main content
Log in

Cognitive potentials in the basal ganglia—frontocortical circuits. An intracerebral recording study

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We studied cognitive functions related to processing sensory and motor activities in the basal ganglia (BG), specifically in the putamen and in cortical structures forming the BG-frontocortical circuits. Intracerebral recordings were made from 160 brain sites in 32 epilepsy surgery candidates. We studied P3-like potentials in five different tests evoked by auditory and visual stimuli, and two sustained potentials that are related to cognitive activities linked with movement preparation: BP (Bereitschaftspotential) and CNV (contingent negative variation). We compared the presence of a potential with a phase reversal or an amplitude gradient to the absence of a generator. All of the studied cognitive potentials were generated in the BG; the occurrence in frontal cortical areas was more selective. The frequency of all but one potential was significantly higher in the BG than in the prefrontal and in the cingulate cortices. The P3-like potentials elicited in the oddball paradigm were also more frequent in the BG than in the motor/premotor cortex, while the occurrence of potentials elicited in motor tasks (BP, CNV, and P3-like potentials in the CNV paradigm) in the motor cortex did not significantly differ from the occurrence in the BG. The processing of motor tasks fits with the model by Alexander et al. of segregated information processing in the motor loop. A variable and task-dependent internal organisation is more probable in cognitive sensory information processing. Cognitive potentials were recorded from all over the putamen. The BG may play an integrative role in cognitive information processing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2a–c
Fig. 3
Fig. 4
Fig. 5a, b

Similar content being viewed by others

References

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Ret Neurosci 9:357–381

    Article  CAS  Google Scholar 

  • Bareš M (2001) Parallel processing of cognitive information in the frontal cortex and the basal ganglia. Homeostasis 41:55–57

    Google Scholar 

  • Bareš M, Rektor I (2001) Basal ganglia involvement in cognitive and sensory processing. A SEEG CNV study in human subjects. Clin Neurophysiol 112:2022–2030

    Article  PubMed  Google Scholar 

  • Baudena P, Halgren E, Heit G, et al (1995) Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Frontal cortex. Electroenceph Clin Neurophysiol 94:251–264

    Article  CAS  PubMed  Google Scholar 

  • Brázdil M, Rektor I, Dufek M, et al (1999) The role of frontal and temporal lobes in visual discrimination task-depth ERP studies. Clin Neurophysiol 29:339–350

    Google Scholar 

  • Brázdil M, Rektor I, Daniel P, et al (2001) Intracerebral event-related potentials to subthreshold target stimuli. Clin Neurophysiol 112:650–661

    Article  PubMed  Google Scholar 

  • Brotchie P, Iansek R, Horne MK (1991) Motor function of the monkey globus pallidus. Brain 114:1685–1702

    PubMed  Google Scholar 

  • Brunia CHM, Damen EJP (1988) Distribution of slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. Electroenceph Clin Neurophysiol 69:234–243

    Article  CAS  PubMed  Google Scholar 

  • Cui RQ, Egkher A, Huter D, et al (2000) High resolution spatiotemporal analysis of the contingent negative variation in simple or complex motor tasks and a non-motor task. Clin Neurophysiol 111:1847–1859

    Article  CAS  PubMed  Google Scholar 

  • Cummings JL (1993) Frontal-subcortical circuits and human behavior. Arch Neurol 50:873–880

    CAS  PubMed  Google Scholar 

  • Dubois B, Malapani C, Verin M, et al (1994) Fonctions cognitives et noyaux gris centraux: Le modele de la maladie de parkinson. Rev Neurol (Paris) 150,11:763–770

    Google Scholar 

  • Goldman-Rakic PS, Selemon LD (1990) New frontiers in basal ganglia research. TINS 13:241–244

    Article  CAS  PubMed  Google Scholar 

  • Graybiel AM (1997) The basal ganglia and cognitive pattern generators. Schizophr Bull 23:459–469

    CAS  PubMed  Google Scholar 

  • Halgren E, Baudena P, Clarke JM, et al (1995a) Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. Electroenceph Clin Neurophysiol 94:191–220

    Article  CAS  PubMed  Google Scholar 

  • Halgren E, Baudena P, Clarke JM (1995b) Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. Electroenceph Clin Neurophysiol 94:229–250

    Article  CAS  PubMed  Google Scholar 

  • Halgren E, Marinkovic K, Chauvel P, et al (1998) Generators of the late cognitive potentials in auditory and visual oddball tasks. Electroenceph Clin Neurophysiol 106:156–164

    Article  CAS  PubMed  Google Scholar 

  • Ikeda A, Luders HO, Burgesss RC, et al (1992) Movement-related potentials recorded from supplementary motor area and primary motor cortex. Brain 115:1017–1043

    PubMed  Google Scholar 

  • Joel D (2001) Open interconnected model of basal ganglia-thalamocortical circuitry and its relevance to the clinical syndrome of Huntington’s disease. Mov Disord 16:407–423

    CAS  PubMed  Google Scholar 

  • Kimura M (1986) The role of primate putamen neurons in the association of sensory stimuli with movement. Neurosci Res 3:436–443

    Article  CAS  PubMed  Google Scholar 

  • Kimura I, Ohnuma A, Seki H, et al (1990) Cognitive impairment in Parkinson’s disease assessed by visuomotor performance system and P300 potential. Tohoku J Exp Med 161:155–165

    Google Scholar 

  • Kornhuber HH, Deecke L (1965) Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen der Menschen: Bereitschaftspotential und reafferente Potentiale. Pflugers Archiv 284:1–17

    CAS  Google Scholar 

  • Kropotov JD, Ponomarev VA (1991) Subcortical neurol correlates of component P300 in man. Electroenceph Clin Neurophysiol 78:40–49

    Article  CAS  PubMed  Google Scholar 

  • Kropotov JD, Etlinger SC, Ponomarev VA, et al (1992a) Event-related neuronal responses in the human strio-pallido-thalamic system. I. Sensory and motor functions. Electroenceph Clin Neurophysiol 84:373–385

    Article  CAS  PubMed  Google Scholar 

  • Kropotov JD, Etlinger SC, Ponomarev VA, et al (1992b) Event-related neuronal responses in the human strio-pallido-thalamic systém. II. Cognitive functions. Electroenceph Clin Neurophysiol 84:386–393

    Article  CAS  PubMed  Google Scholar 

  • Lamarche M, Louvel J, Buser P, Rektor I (1995) Intracerebral recordings of slow potentials in a contingent negative variation paradigm: an exploration in epileptic patients: Electroenceph Clin Neurophysiol 95:268–276

    Google Scholar 

  • Libet B (1985) Unconscious cerebral initiative and the role of conscious will in voluntary action. Behav Brain Sci 8:529–566

    Google Scholar 

  • Marsden CD (1980) The enigma of the basal ganglia and movement. TINS 3:284–287

    Google Scholar 

  • Middleton FA, Strick PL (2000) Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain and Cognition 42:183–200

    Article  CAS  PubMed  Google Scholar 

  • Parent A, Cicchetti F (1998) The current model of basal ganglia organization under scrutiny. Mov Disord 13:199–202

    CAS  PubMed  Google Scholar 

  • Parent A, Lévesque M, Parent M (2001) A re-evaluation of the current model of the basal ganglia. Parkinsonism&Related Disord 7:193–198

    Google Scholar 

  • Rektor I (2000) Long-lasting simultaneous activation of cortical and subcortical in movement preparation and execution. Clinical neurophysiology at the beginning of the 21st century. Clin Neurophysiol 53[Suppl]: 192–195

  • Rektor I (2002) Scalp-recorded Bereitschaftspotential is the result of the activity of cortical and subcortical generators—a hypothesis. Clin Neurophysiol 113:1998–2005

    Article  PubMed  Google Scholar 

  • Rektor I, Feve A, Buser P, et al (1994) Intracerebral recording of movement related readiness potentials in epileptic patients: Electroenceph Clin Neurophysiol 90:273–283

    Google Scholar 

  • Rektor I, Louvel J, Lamarche M (1998) Intracerebral recording of potentials accompanying simple limb movements: a SEEG study in epileptic patients: Electroenceph Clin Neurophysiol 107:227–286

    Google Scholar 

  • Rektor I, Kaňovský P, Bareš M, Louvel J, Lamarche, M (2001a) Evoked potentials, ERP, CNV, readiness potential, and movement accompanying potential recorded from the posterior thalamus in human subjects. A SEEG study. Clin Neurophysiol 31:1–9

    Google Scholar 

  • Rektor I, Bareš M, Kaňovský P, Kukleta M (2001b) Intracerebral recording of readiness potential induced by a complex motor task. Mov Disord 16:698–704

    Article  CAS  PubMed  Google Scholar 

  • Rektor I, Bareš M, Kubová D (2001c) Movement-related potentials in the basal ganglia: a SEEG readiness potential study. Clin Neurophysiol 112:2146–2153

    Article  CAS  PubMed  Google Scholar 

  • Rektor I, Kaňovský P, Bareš M, Brázdil M, Streitová H, Klajblová I, Kuba R, Daniel P (2003) A SEEG study of ERP in motor and premotor cortices and in the basal ganglia. Clin Neurophysiol 114:463–471

    Article  CAS  PubMed  Google Scholar 

  • Romo R, Scarnati E, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. II. Movement-related activity in the anterior striatum. Exp Brain Res 91:385–395

    CAS  PubMed  Google Scholar 

  • Stein S, Volpe BT (1983) Classical “parietal” neglect syndrome after subcortical right frontal lobe infarction. Neurology 33:797–799

    CAS  PubMed  Google Scholar 

  • Takada M, Tokuno H, Nambu A, et al. (1998) Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex. Exp Brain Res 120:114–128

    CAS  PubMed  Google Scholar 

  • Talairach J, Szikla G, Tournoux P, et al (1967) Atlas d’anatomie stereotactique du telencephale. Masson, Paris

  • Vaughan HG, Weinberg H, Lehmann D, et al (1986) Approaches to defining the intracranial generators of event-related electrical and magnetic fields. In: McCallum WC, Zappoli R, Denoth F (eds) Cerebral psychophysiology: studies in event-related potentials. EEG. Elsevier, Paris, pp 505–544

  • Verleger R, Wascher E, Wauschkuhn B, et al (1999) Consequences of altered cerebellar input for the cortical regulation of motor coordination, as reflected in EEG potentials. Exp Brain Res 127:409–422

    CAS  PubMed  Google Scholar 

  • Walter WG, Cooper R, Aldridge VJ, et al (1964) The contingent negative variation: an electro-cortical sign of sensorimotor association in man. Electroenceph Clin Neurophysiol 17:340–344

    Google Scholar 

Download references

Acknowledgement

Supported by research program MŠ ČR 112801.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ivan Rektor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rektor, I., Bareš, M., Kaňovský, P. et al. Cognitive potentials in the basal ganglia—frontocortical circuits. An intracerebral recording study. Exp Brain Res 158, 289–301 (2004). https://doi.org/10.1007/s00221-004-1901-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-004-1901-6

Keywords

Navigation