Skip to main content
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 Dec 20;91(26):12467–12471. doi: 10.1073/pnas.91.26.12467

Visual motion induces synchronous oscillations in turtle visual cortex.

J C Prechtl 1
PMCID: PMC45459  PMID: 7809060

Abstract

In mammalian brains, multielectrode recordings during sensory stimulation have revealed oscillations in different cortical areas that are transiently synchronous. These synchronizations have been hypothesized to support integration of sensory information or represent the operation of attentional mechanisms, but their stimulus requirements and prevalence are still unclear. Here I report an analogous synchronization in a reptilian cortex induced by moving visual stimuli. The synchronization, as measured by the coherence function, applies to spindle-like 20-Hz oscillations recorded with multiple electrodes implanted in the dorsal cortex and the dorsal ventricular ridge of the pond turtle. Additionally, widespread increases in coherence are observed in the 1- to 2-Hz band, and widespread decreases in coherence are seen in the 10- and 30- to 45-Hz bands. The 20-Hz oscillations induced by the moving bar or more natural stimuli are nonstationary and can be sustained for seconds. Early reptile studies may have interpreted similar spindles as electroencephalogram correlates of arousal; however, the absence of these spindles during arousing stimuli in the dark suggests a more specific role in visual processing. Thus, visually induced synchronous oscillations are not unique to the mammalian cortex but also occur in the visual area of the primitive three-layered cortex of reptiles.

Full text

PDF
12469

Selected References

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

  1. Bekisz M., Wróbel A. 20 Hz rhythm of activity in visual system of perceiving cat. Acta Neurobiol Exp (Wars) 1993;53(1):175–182. [PubMed] [Google Scholar]
  2. Bouyer J. J., Montaron M. F., Vahnée J. M., Albert M. P., Rougeul A. Anatomical localization of cortical beta rhythms in cat. Neuroscience. 1987 Sep;22(3):863–869. doi: 10.1016/0306-4522(87)92965-4. [DOI] [PubMed] [Google Scholar]
  3. Bouyer J. J., Tilquin C., Rougeul A. Thalamic rhythms in cat during quiet wakefulness and immobility. Electroencephalogr Clin Neurophysiol. 1983 Feb;55(2):180–187. doi: 10.1016/0013-4694(83)90186-4. [DOI] [PubMed] [Google Scholar]
  4. Bressler S. L., Coppola R., Nakamura R. Episodic multiregional cortical coherence at multiple frequencies during visual task performance. Nature. 1993 Nov 11;366(6451):153–156. doi: 10.1038/366153a0. [DOI] [PubMed] [Google Scholar]
  5. Bullock T. H., Hofmann M. H., Nahm F. K., New J. G., Prechtl J. C. Event-related potentials in the retina and optic tectum of fish. J Neurophysiol. 1990 Sep;64(3):903–914. doi: 10.1152/jn.1990.64.3.903. [DOI] [PubMed] [Google Scholar]
  6. Bullock T. H., Karamürsel S., Hofmann M. H. Interval-specific event related potentials to omitted stimuli in the electrosensory pathway in elasmobranchs: an elementary form of expectation. J Comp Physiol A. 1993 May;172(4):501–510. doi: 10.1007/BF00213532. [DOI] [PubMed] [Google Scholar]
  7. Eckhorn R., Bauer R., Jordan W., Brosch M., Kruse W., Munk M., Reitboeck H. J. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern. 1988;60(2):121–130. doi: 10.1007/BF00202899. [DOI] [PubMed] [Google Scholar]
  8. Eckhorn R., Frien A., Bauer R., Woelbern T., Kehr H. High frequency (60-90 Hz) oscillations in primary visual cortex of awake monkey. Neuroreport. 1993 Mar;4(3):243–246. doi: 10.1097/00001756-199303000-00004. [DOI] [PubMed] [Google Scholar]
  9. Engel Andreas K., König Peter, Gray Charles M., Singer Wolf. Stimulus-Dependent Neuronal Oscillations in Cat Visual Cortex: Inter-Columnar Interaction as Determined by Cross-Correlation Analysis. Eur J Neurosci. 1990;2(7):588–606. doi: 10.1111/j.1460-9568.1990.tb00449.x. [DOI] [PubMed] [Google Scholar]
  10. FREEMAN W. J. Distribution in time and space of prepyriform electrical activity. J Neurophysiol. 1959 Nov;22:644–665. doi: 10.1152/jn.1959.22.6.644. [DOI] [PubMed] [Google Scholar]
  11. Freeman W. J., Skarda C. A. Spatial EEG patterns, non-linear dynamics and perception: the neo-Sherringtonian view. Brain Res. 1985 Dec;357(3):147–175. doi: 10.1016/0165-0173(85)90022-0. [DOI] [PubMed] [Google Scholar]
  12. Freeman W. J., van Dijk B. W. Spatial patterns of visual cortical fast EEG during conditioned reflex in a rhesus monkey. Brain Res. 1987 Oct 6;422(2):267–276. doi: 10.1016/0006-8993(87)90933-4. [DOI] [PubMed] [Google Scholar]
  13. Gray C. M., Engel A. K., König P., Singer W. Synchronization of oscillatory neuronal responses in cat striate cortex: temporal properties. Vis Neurosci. 1992 Apr;8(4):337–347. doi: 10.1017/s0952523800005071. [DOI] [PubMed] [Google Scholar]
  14. Gray C. M., König P., Engel A. K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989 Mar 23;338(6213):334–337. doi: 10.1038/338334a0. [DOI] [PubMed] [Google Scholar]
  15. Gray C. M., Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1698–1702. doi: 10.1073/pnas.86.5.1698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gray Charles M., Engel Andreas K., König Peter, Singer Wolf. Stimulus-Dependent Neuronal Oscillations in Cat Visual Cortex: Receptive Field Properties and Feature Dependence. Eur J Neurosci. 1990;2(7):607–619. doi: 10.1111/j.1460-9568.1990.tb00450.x. [DOI] [PubMed] [Google Scholar]
  17. HUNSAKER D., 2nd, LANSING R. W. Electroencephalographic studies of reptiles. J Exp Zool. 1962 Feb;149:21–32. doi: 10.1002/jez.1401490103. [DOI] [PubMed] [Google Scholar]
  18. Huntley A. C. Electrophysiological and behavioral correlates of sleep in the desert iguana, Dipsosaurus dorsalis Hallowell. Comp Biochem Physiol A Comp Physiol. 1987;86(2):325–330. doi: 10.1016/0300-9629(87)90338-0. [DOI] [PubMed] [Google Scholar]
  19. Kreiter A. K., Singer W. Oscillatory Neuronal Responses in the Visual Cortex of the Awake Macaque Monkey. Eur J Neurosci. 1992;4(4):369–375. doi: 10.1111/j.1460-9568.1992.tb00884.x. [DOI] [PubMed] [Google Scholar]
  20. Lopes da Silva F. H., van Rotterdam A., Storm van Leeuwen W., Tielen A. M. Dynamic characteristics of visual evoked potentials in the dog. II. Beta frequency selectivity in evoked potentials and background activity. Electroencephalogr Clin Neurophysiol. 1970 Sep;29(3):260–268. doi: 10.1016/0013-4694(70)90138-0. [DOI] [PubMed] [Google Scholar]
  21. Murthy V. N., Fetz E. E. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5670–5674. doi: 10.1073/pnas.89.12.5670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Neuenschwander S., Varela F. J. Visually triggered neuronal oscillations in the pigeon: an autocorrelation study of tectal activity. Eur J Neurosci. 1993 Jul 1;5(7):870–881. doi: 10.1111/j.1460-9568.1993.tb00939.x. [DOI] [PubMed] [Google Scholar]
  23. Niebur E., Koch C., Rosin C. An oscillation-based model for the neuronal basis of attention. Vision Res. 1993 Dec;33(18):2789–2802. doi: 10.1016/0042-6989(93)90236-p. [DOI] [PubMed] [Google Scholar]
  24. Prechtl J. C., Bullock T. H. Barbiturate sensitive components of visual ERPs in a reptile. Neuroreport. 1992 Sep;3(9):801–804. doi: 10.1097/00001756-199209000-00020. [DOI] [PubMed] [Google Scholar]
  25. Prechtl J. C., Bullock T. H. Event-related potentials to omitted visual stimuli in a reptile. Electroencephalogr Clin Neurophysiol. 1994 Jul;91(1):54–66. doi: 10.1016/0013-4694(94)90018-3. [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