Cellular Mechanisms of Visually Evoked Oscillations

How does the cerebral cortex process sensory information? We now know that this seemingly simple problem is met by a system of interconnected neurons that is truely awe-inspiring in its complexity, yet, at the same time beautiful in its simplicity. The cerebral cortex is complex in that its components are massively interconnected in a mixed parallel/serial network, yet in some ways it is simple in that the cortex is built up, at least in part, of a repeating mosaic of elementary circuits (e.g. columns or modules) that utilize the same basic components (e.g. pyramidal and non-pyramidal cells).

A long sought goal of Neuroscience has been to understand, at a cellular and synaptic level, the mechanisms by which the cerebral cortex, or even a single cortical column, operates. The degree of difficulty in attempting to unravel the cellular mechanisms by which the cerebral cortex operates is directly proportional to the degree to which the cells of the cortex operate as individual units. In some states, such as slow wave sleep, circuits of cortical and thalamic neurons interact in a relatively simple manner in the generation of the slow electroencephalographic rhythms of sleep (Steriade, McCormick and Sejnowski, 1993). While in others, such as during the processing of a complex visual scene during behaviour, cortical neurons respond to individual components of the sensory inputs within well defined locations in space, as well as to more global variables (e.g. Hubel and Wiesel, 1977). In a gross oversimplification, it had often been assumed that these two types of activity were quite distinct: synchronized rhythmic oscillations were the manner in which the brain "hummed" while it was asleep, while de-synchronized activity demoninated whenever the brain was actively processing incoming sensory information. The pattern of activity generated during active sensory processing was believed to be anything but synchronized oscillations.

The observation of pronounced synchronized oscillations in the cerebral cortex during the presentation of sensory stimuli in the olfactory system (Freeman, 1987), as well as the occurrence of higher frequency oscillations (30-70 Hz) in the frontal cortex in awake and attentive animals (Bouyer et al., 1987) suggested that coordinated, synchronized activity may actually play an important role in the normal operation of the cerebral cortex.

Indeed, extracellular recordings from neurons in the cat visual cortex in vivo revealed that a subset of cells generates a pattern of repetitive burst discharges during the presentation of a visual stimulus (Gray et al., 1990).

• Bouyer, J.J., Montaron, M.F., Vahnee, M.P., Albert, M.P. and Rougeul, A. (1987) Neuroscience 22: 863-869.
• Freeman, W.J. (1987) in Handbook of Electroencephalography and Clinical Neurophysiology, Eds. Gevins and Remond (Elsevier, Amsterdam), Vol. 3A, part 2, Chapter 14.
• Gray, C.M., Engel, A.K., Konig, P., and Singer, W. (1990) Stimulus-dependent neuronal oscillations in cat visual cortex: receptive field properties and feature dependence. Eur. J. Neurosci. 2: 607-619.
  
• Hubel, D.H. and Wiesel, T.N. (1977) Functional architecture of macaque visual cortex. Prox. R. Soc. Lond. B. 198: 1-59.
  
• Steriade, M., McCormick,D.A., and Sejnowski, T. (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.