Experimental Brain Research

, Volume 86, Issue 3, pp 641–651

The role of the subthalamic nucleus in the response of globus pallidus neurons to stimulation of the prelimbic and agranular frontal cortices in rats

  • L. J. Ryan
  • K. B. Clark
Article

Summary

We investigated how the cerebral cortex can influence the globus pallidus by two routes: the larger, net inhibitory route through the neostriatum and the separate, smaller, net excitatory route through the subthalamic nucleus. Stimulation (0.3 and 0.7 mA) of two regions of frontal agranular (motor) cortex and of the medial orbitofrontal cortex centered in the prelimbic cortex typically elicited one or more of the following extracellularly recorded responses in over 50% of tested cells: an initial excitation (approximately 6 ms latency), a short inhibition (15 ms latency) and a late excitation (29 ms latency). Some other cells responded with an excitatory response only (18 ms latency). The excitatory responses largely arise from the subthalamic route. Kainic acid or electrolytic lesion of the subthalamic nucleus eliminated most excitatory responses and greatly prolonged the duration (16 vs 50 ms) of the inhibition. Subthalamic neurons typically showed one or more of the following responses to cortical stimulation: an early excitatory response (4 ms latency), an inhibitory period (9 ms) and a late excitatory response (16 ms). The early response was seen after motor cortex but not prelimbic stimulation. The timing of the globus pallidus and subthalamic responses suggest the operation of a reciprocal inhibitory/excitatory pathway. Two reciprocal interactions were indicated. First, pallidal inhibition may disinhibit the subthalamus and, via a feedback pathway onto the same pallidal cells, act to terminate the neostriatal-induced inhibition. Second, there may be a feedforward pathway from pallidal cells to subthalamic neurons to a different group of pallidal cells. This pathway could act to suppress competing responses. Thus the subthalamus may have three actions: 1) an early direct cortical and 2,3) later reciprocal feedforward and feedback excitatory antagonism of the neostriatal mediated inhibition of globus pallidus.

Key words

Subthalamus Globus pallidus Prelimbic cortex Motor cortex Basal ganglia 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albin RL, Young AB, Penny JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375CrossRefPubMedGoogle Scholar
  2. Alexander GE, DeLong M (1985) Microstimulation of the primate neostriatum. I. Physiological properties of striatal microexcitable zones. J Neurophysiol 53:1401–1416Google Scholar
  3. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 9:357–381Google Scholar
  4. Bergman H, Wichmann T DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436–1438PubMedGoogle Scholar
  5. Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA (1990) Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde peroxidase study in the rat. Brain Res 513:43–59Google Scholar
  6. Chevalier G, Vacher S, Deniau JM, Desban M (1985) Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tectodiencephalic neurons. Brain Res 334:215–226Google Scholar
  7. Deniau JM, Hammond C, Chevalier G, Feger J (1978) Evidence for branched subthalamic nucleus projections to substantia nigra, entopeduncular nucleus and globus pallidus. Neurosci Lett 9:117–121Google Scholar
  8. Deniau JM, Feger J, LeGuyader C (1976) Striatal-evoked inhibition of identified nigrothalamic neurons. Brain Res 104:152–156Google Scholar
  9. Divac J, Fonnum F, Storm-Mathisen J (1977) High affinity uptake of glutamate in terminals of corticostriatal axons. Nature 266:377–378Google Scholar
  10. Donoghue JP, Herkenham M (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 365:397–403Google Scholar
  11. Donoghue JP, Kitai ST (1981) A collateral pathway to the neostriatum from corticofugal neurons of the rat sensory motor cortex: An intracellular HRP study. J Comp Neurol 210:1–13Google Scholar
  12. Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neorstriatum. J Comp Neurol 267:455–471Google Scholar
  13. Fonnum F, Gottesfeld Z, Grofova I (1978) Distribution of glutamate decarboxylase, choline acetyltransferase and aromatic amino acid decarboxylase in the basal ganglia of normal and operated rats: evidence for striato-pallidal, striato-entopeduncular, and striato-nigral GABAergic fibers. Brain Res 143:125–138Google Scholar
  14. Fujimoto K, Kita H (1990) Unit responses recorded in the substantia nigra after stimulation of the frontal cortex. Soc Neurosci Abstr 16:237Google Scholar
  15. Fuller JH, Schlag JD (1976) Determination of antidromic excitation by the collision test; problems of interpretation. Brain Res 112:283–298Google Scholar
  16. Gerfen CR (1989) The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246:382–388Google Scholar
  17. Gerfen CR, Young WS (1988) Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res 460:161–167Google Scholar
  18. Giufrida R, LiVolsi G, Maugeri G, Perciavalle V (1985) Influences of pyramidal tract on the subthalamic nucleus in the cat. Neurosci Lett 54:231–235Google Scholar
  19. Gonya-Magee T, Anderson ME (1983) An electrophysiological characterization of projections from the pedunculopontine area to the entopeduncular nucleus and globus pallidus in the cat. Exp Brain Res 49:269–279Google Scholar
  20. Groenewegen HJ, Berendse HW (1990) Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol 294:607–622PubMedGoogle Scholar
  21. Jinnai K, Matsuda Y (1979) Neurons of the motor cortex projecting commonly on the caudate nucleus and the lower brainstem in the cat. Neurosci Lett 13:121–126Google Scholar
  22. Kita H (1990) Intracellular responses recorded in the globus pallidus after stimulation of the frontal cortex (CX), the neostriatum (Str), the subthalamic nucleus (STH) and the substantia nigra (SN). Soc Neurosci Abstr 16:427Google Scholar
  23. Kita H, Kitai ST (1987) Efferent projections of the subthalamic in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260:435–452Google Scholar
  24. Kita H, Chang HT, Kitai ST (1983) Pallidal inputs to subthalamus: intracellular analysis. Brain Res 264:255–265Google Scholar
  25. Kita H, Kitai ST (1988) Glutamate decarboxylase immunoreactive neurons in rat neostriatum: their morphological types and populations. Brain Res 447:346–352Google Scholar
  26. Kitai ST, Deniau JM (1981) Cortical inputs to the subthalamus: intracellular analysis. Brain Res 214:411–415Google Scholar
  27. Kitai ST, Kita H (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In: Carpenter MB, Jaraman A (eds) The basal ganglia II. Structure and function: current concepts. Plenum Press, New York, pp 357–373Google Scholar
  28. Kitai ST, Kocsis JD, Preston RJ, Sugimori M (1976) Monosynaptic inputs to caudate neurons identified by intracellular injection of horseradish peroxidase. Brain Res 109:601–606Google Scholar
  29. Levine MS, Hull CD, Buchwald NA (1974) Pallidal and entopeduncular intracellular responses to striatal, cortical, thalamic, and sensory inputs. Exp Neurol 44:448–460Google Scholar
  30. McGeer PL, McGeer EG, Scherer V, Singh K (1977) A glutamatergic corticostriatal path? Brain Res 128:369–373Google Scholar
  31. Nakanishi H, Kita H, Kitai ST (1987) Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro preparations: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res 437:45–55Google Scholar
  32. Nauta HJ, Cuenod M (1982) Perikaryal cell labeling in the subthalamic nucleus following injection of 3H-gamma-aminobutyric acid into the pallidal complex: an autoradiographic study in the cat. Neuroscience 7:2725–2734Google Scholar
  33. Noda H, Manohar S, Adey WR (1968) Responses of cat pallidal neurons to cortical and subcortical stimuli. Exp Neurol 20:585–610Google Scholar
  34. Ohye C, Le Guyader C, Feger J (1976) Responses of subthalamic and pallidal neurons to striatal stimulation: an extracellular study on awake monkeys. Brain Res 111:241–252Google Scholar
  35. Parent A, Hazrati LN, Smith Y (1989) The subthalamic nucleus in primates. A neuroanatomical and immunohistochemical study. In: Crossman AR, Sambrook MA (eds) Neural mechanisms in disorders of movement, current problems in neurology, Vol 9. Libbey Press, London, pp 29–35Google Scholar
  36. Park MR, Falls WM, Kitai ST (1982) An intracellular HRP study of the rat globus pallidus. I. Responses and light microscopic analysis. J Comp Neurol 211:284–294Google Scholar
  37. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. 2nd edn. Academic Press, SydneyGoogle Scholar
  38. Penny GR, Afsharpour S, Kitai ST (1986) The glutamate decarboxylase-, leucine enkephalin-, methionine enkephalin- and substance P-immunoreactive neurons in the neostriatum of the rat and cat: evidence for partial population overlap. Neuroscience 17:1011–1045Google Scholar
  39. Reinoso-Suarez F, Llamas A, Avendaño C (1982) Pallido-cortical projections in the cat studied by means of the horseradish peroxidase retrograde transport technique. Neurosci Lett 29:225–229Google Scholar
  40. Rinvik E, Grofova I, Hammond C, Feger J, Deniau JM (1979) A study of the afferent connections to the subthalamic nucleus in the monkey and the cat using the HRP technique. Adv Neurol 24:53–70Google Scholar
  41. Robledo P, Feger J (1990) Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data. Brain Res 518:47–54Google Scholar
  42. Rouzaire-Dubois B, Hammond C, Hamon B, Feger J (1980) Pharmacological blockade of the globus pallidus-induced inhibitory response of subthalamic cells in the rat. Brain Res 200:321–329Google Scholar
  43. Rozuaire-Dubois B, Scarnati E (1985) Bilateral corticosubthalamic nucleus projections: electophysiological study in rats with chronic cerebral lesions. Neuroscience 15:69–79Google Scholar
  44. Ryan LJ, Tepper JM, Young SJ, Groves PM (1986) Frontal cortex stimulation evoked neostriatal potentials in rats: intracellular and extracellular analysis. Brain Res Bull 17:751–758Google Scholar
  45. Toan DL, Schultz W (1985) Responses of rat pallidum cells to cortex stimulation and effects of altered dopaminergic activity. Neuroscience 15:683–694Google Scholar
  46. Tremblay L, Filion M (1990) Behavioral and neuronal effects of GABA agonist and antagonist injected locally in the globus pallidus of intact monkeys. Soc Neurosci Abstr 16:428Google Scholar
  47. Van der Kooy D, Kolb B (1985) Non-cholinergic globus pallidus cells that project to the cortex but not to the subthalamic nucleus in rat. Neurosci Lett 57:113–118Google Scholar
  48. Wilson CJ (1987) Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol 263:567–580Google Scholar
  49. Zilles K (1985) The cortex of the rat. Springer, BerlinGoogle Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • L. J. Ryan
    • 1
  • K. B. Clark
    • 1
  1. 1.Department of PsychologyOregon State UniversityCorvallisUSA

Personalised recommendations