Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Apr 26;91(9):4009–4013. doi: 10.1073/pnas.91.9.4009

Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex.

F A Wilson 1, S P O'Scalaidhe 1, P S Goldman-Rakic 1
PMCID: PMC43712  PMID: 8171027

Abstract

The responses of putative gamma-aminobutyratergic interneurons (fast-spiking) and pyramidal (regular-spiking) cell pairs were compared in monkeys performing visual and memory-guided oculomotor tasks. Both fast- and regular-spiking neurons had similar receptive fields, indicating that gamma-aminobutyratergic interneurons carry a specific informational signal, as opposed to providing nonspecific modulation. However, the responses of the pairs were inverted and the timing of excitatory and inhibitory responses appeared to be phased, a property consistent with gamma-aminobutyrate-mediated shaping of receptive fields. These observations (i) provide evidence that interneurons and pyramidal cells can be differentiated in vivo and (ii) begin to elucidate the role of gamma-aminobutyratergic mechanisms in cognition.

Full text

PDF
4009

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barbas H. Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol. 1988 Oct 15;276(3):313–342. doi: 10.1002/cne.902760302. [DOI] [PubMed] [Google Scholar]
  2. Bruce C. J., Goldberg M. E. Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol. 1985 Mar;53(3):603–635. doi: 10.1152/jn.1985.53.3.603. [DOI] [PubMed] [Google Scholar]
  3. Cavada C., Goldman-Rakic P. S. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol. 1989 Sep 22;287(4):422–445. doi: 10.1002/cne.902870403. [DOI] [PubMed] [Google Scholar]
  4. Celio M. R. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science. 1986 Feb 28;231(4741):995–997. doi: 10.1126/science.3945815. [DOI] [PubMed] [Google Scholar]
  5. Connors B. W., Gutnick M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 1990 Mar;13(3):99–104. doi: 10.1016/0166-2236(90)90185-d. [DOI] [PubMed] [Google Scholar]
  6. Douglas R. J., Martin K. A. A functional microcircuit for cat visual cortex. J Physiol. 1991;440:735–769. doi: 10.1113/jphysiol.1991.sp018733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dykes R. W., Landry P., Metherate R., Hicks T. P. Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J Neurophysiol. 1984 Dec;52(6):1066–1093. doi: 10.1152/jn.1984.52.6.1066. [DOI] [PubMed] [Google Scholar]
  8. Ellaway P. H. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol. 1978 Aug;45(2):302–304. doi: 10.1016/0013-4694(78)90017-2. [DOI] [PubMed] [Google Scholar]
  9. Ferino F., Thierry A. M., Saffroy M., Glowinski J. Interhemispheric and subcortical collaterals of medial prefrontal cortical neurons in the rat. Brain Res. 1987 Aug 11;417(2):257–266. doi: 10.1016/0006-8993(87)90450-1. [DOI] [PubMed] [Google Scholar]
  10. Freund T. F., Martin K. A., Somogyi P., Whitteridge D. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y- type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation. J Comp Neurol. 1985 Dec 8;242(2):275–291. doi: 10.1002/cne.902420209. [DOI] [PubMed] [Google Scholar]
  11. Funahashi S., Bruce C. J., Goldman-Rakic P. S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol. 1989 Feb;61(2):331–349. doi: 10.1152/jn.1989.61.2.331. [DOI] [PubMed] [Google Scholar]
  12. Hendry S. H., Schwark H. D., Jones E. G., Yan J. Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci. 1987 May;7(5):1503–1519. doi: 10.1523/JNEUROSCI.07-05-01503.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kawaguchi Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol. 1993 Feb;69(2):416–431. doi: 10.1152/jn.1993.69.2.416. [DOI] [PubMed] [Google Scholar]
  14. Knowles W. D., Schwartzkroin P. A. Local circuit synaptic interactions in hippocampal brain slices. J Neurosci. 1981 Mar;1(3):318–322. doi: 10.1523/JNEUROSCI.01-03-00318.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lewis D. A., Lund J. S. Heterogeneity of chandelier neurons in monkey neocortex: corticotropin-releasing factor- and parvalbumin-immunoreactive populations. J Comp Neurol. 1990 Mar 22;293(4):599–615. doi: 10.1002/cne.902930406. [DOI] [PubMed] [Google Scholar]
  16. Martin K. A. The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol. 1988 Sep;73(5):637–702. doi: 10.1113/expphysiol.1988.sp003190. [DOI] [PubMed] [Google Scholar]
  17. McCormick D. A., Connors B. W., Lighthall J. W., Prince D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 1985 Oct;54(4):782–806. doi: 10.1152/jn.1985.54.4.782. [DOI] [PubMed] [Google Scholar]
  18. Mikami A., Ito S., Kubota K. Visual response properties of dorsolateral prefrontal neurons during visual fixation task. J Neurophysiol. 1982 Apr;47(4):593–605. doi: 10.1152/jn.1982.47.4.593. [DOI] [PubMed] [Google Scholar]
  19. Mountcastle V. B., Talbot W. H., Sakata H., Hyvärinen J. Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol. 1969 May;32(3):452–484. doi: 10.1152/jn.1969.32.3.452. [DOI] [PubMed] [Google Scholar]
  20. Park T. J., Pollak G. D. GABA shapes a topographic organization of response latency in the mustache bat's inferior colliculus. J Neurosci. 1993 Dec;13(12):5172–5187. doi: 10.1523/JNEUROSCI.13-12-05172.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pirot S., Godbout R., Mantz J., Tassin J. P., Glowinski J., Thierry A. M. Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: evidence for the involvement of both dopaminergic and GABAergic components. Neuroscience. 1992 Aug;49(4):857–865. doi: 10.1016/0306-4522(92)90362-6. [DOI] [PubMed] [Google Scholar]
  22. Richardson R. T., DeLong M. R. Context-dependent responses of primate nucleus basalis neurons in a go/no-go task. J Neurosci. 1990 Aug;10(8):2528–2540. doi: 10.1523/JNEUROSCI.10-08-02528.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schultz W. Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. J Neurophysiol. 1986 Nov;56(5):1439–1461. doi: 10.1152/jn.1986.56.5.1439. [DOI] [PubMed] [Google Scholar]
  24. Schwartz M. L., Zheng D. S., Goldman-Rakic P. S. Periodicity of GABA-containing cells in primate prefrontal cortex. J Neurosci. 1988 Jun;8(6):1962–1970. doi: 10.1523/JNEUROSCI.08-06-01962.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schwartzkroin P. A., Kunkel D. D. Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J Comp Neurol. 1985 Feb 8;232(2):205–218. doi: 10.1002/cne.902320206. [DOI] [PubMed] [Google Scholar]
  26. Schwartzkroin P. A., Mathers L. H. Physiological and morphological identification of a nonpyramidal hippocampal cell type. Brain Res. 1978 Nov 17;157(1):1–10. doi: 10.1016/0006-8993(78)90991-5. [DOI] [PubMed] [Google Scholar]
  27. Simons D. J. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol. 1978 May;41(3):798–820. doi: 10.1152/jn.1978.41.3.798. [DOI] [PubMed] [Google Scholar]
  28. Swadlow H. A. Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties. J Neurophysiol. 1988 Apr;59(4):1162–1187. doi: 10.1152/jn.1988.59.4.1162. [DOI] [PubMed] [Google Scholar]
  29. Wilson F. A., Rolls E. T. Neuronal responses related to reinforcement in the primate basal forebrain. Brain Res. 1990 Feb 19;509(2):213–231. doi: 10.1016/0006-8993(90)90546-n. [DOI] [PubMed] [Google Scholar]
  30. Wilson F. A., Scalaidhe S. P., Goldman-Rakic P. S. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science. 1993 Jun 25;260(5116):1955–1958. doi: 10.1126/science.8316836. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES