Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex.

Abstract

In areas 17 and 18 of the cat visual cortex the firing probability of neurons, in response to the presentation of optimally aligned light bars within their receptive field, oscillates with a peak frequency near 40 Hz. The neuronal firing pattern is tightly correlated with the phase and amplitude of an oscillatory local field potential recorded through the same electrode. The amplitude of the local field-potential oscillations are maximal in response to stimuli that match the orientation and direction preference of the local cluster of neurons. Single and multiunit recordings from the dorsal lateral geniculate nucleus of the thalamus showed no evidence of oscillations of the neuronal firing probability in the range of 20-70 Hz. The results demonstrate that local neuronal populations in the visual cortex engage in stimulus-specific synchronous oscillations resulting from an intracortical mechanism. The oscillatory responses may provide a general mechanism by which activity patterns in spatially separate regions of the cortex are temporally coordinated.The mechanism by which populations of neurons in the cerebral cortex temporally coordinate their activity patterns in response to specific sensory stimuli constitutes a basic unresolved question in sensory physiology. In the vertebrate olfactory system the spatiotemporal coordination of neuronal activity is achieved by the synchronization of oscillatory responses having a frequency in the range of 40-80 Hz (1-5). Evidence suggesting that a similar mechanism for the synchronization of activity may operate in the neocortex has come from field potential recordings in awake animals. It has been demonstrated that oscillatory activity in the high betafrequency range (20-50 Hz) occurs in sensory areas of the neocortex when the animals direct their attention to meaningful stimuli (6-11).Previously we have discovered, from recordings in area 17 of awake kittens, that neuronal responses recorded during periods of behavioral attention exhibit a rhythmic firing pattern that is tightly correlated with an oscillatory local field potential (LFP) having a frequency near 40 Hz (12). Thus, we sought to determine whether the oscillatory responses could also be recorded under varying conditions of anesthesia that would permit a more quantitative analysis of both their stimulus specificity as well as their temporal properties. Here, we extend our previous observations (13) and report that local groups of neurons, within functional columns ofthe visual cortex, engage in stimulus-specific oscillatory responses having a frequency near 40 Hz. This periodic neuronal activity is tightly correlated to the simultaneously recorded LFP, which in the majority of recordings has a similar orientation and direction preference as the local cluster of neurons. No comparable oscillations of firing probability were found for the thalamic input to visual cortex, indicating that the generation of oscillatory responses is a cortical phenomenon. The results suggest the hypothesis that the temporal pat...

The complementary brain: unifying brain dynamics and modularity

“…Indeed, relative activities need to be computed synchronously, and early theorems about short-term memory and long-term memory processing 67 predicted an important role for synchronous processing between the interacting cells. Subsequent neurophysiological experiments have emphasized the functional importance of synchronous brain states 86,87 . More recent neural modeling has shown how such synchronized activity patterns can, for example, quantitatively explain psychophysical data about temporal order judgments during perceptual grouping within the visual cortex 88 .…”

The role of oscillatory brain activity in object processing and figure–ground segmentation in human vision

“…It is clear that 76 hierarchical processing must play some role in the formation of coherent percepts, for it is 77 known from the pioneering work of Wiesel (1962, 1968) More recently, it has been hypothesized that coherent percepts may arise from 87 synchronized spike activity between neurons that code features of the same object. The 88 binding-by-synchronization model, which attributes roles to both feedforward and feedback 89 processes, has been advanced largely on the basis of animal studies (Eckhorn,et al,90 1988; Gray & Singer, 1989;Kreiter & Singer, 1996;W Singer, 2007). Our goal in this paper 91 was to make use of the spatio-temporal resolution offered by the neuroimaging technique 92 of magnetoencephalography (MEG) to assess the synchronization model of object 93 processing in human vision.…”

Oscillatory Brain Dynamics, Wavelet Analysis, and Cognition

“…For further studies of evoked electric and magnetic 40-Hz activity see, e.g., Galambos, Makeig, & Talmachoff (1981), Pantev et al (1991), and Ribary et al (1992). A large number of studies at the single-cell level complement these results (Llinás, 1988;Gray & Singer, 1987;Gray, König, Engel, & Singer, 1989;Eckhorn et al, 1988). The concept of evoked and induced rhythms ) is a further approach parallel to frequency analysis and resonance phenomena.…”

“…This statement is strongly based on cognitive experiments by means of single and multiple unit activity and field potentials in animals, event related potentials and EEG in humans, and a great variety of clinical studies by use of modern imaging techniques. The distributed alpha responses as reported here may add a further aspect to this problem which has so far been dominated by the widely discussed role of gamma responses for this process of perceptual binding (Gray & Singer, 1987;Gray et al, 1989;Eckhorn et al, 1988; for an overview including results at the EEG level, see, e.g., .…”

“…Recent findings by Gray and colleagues (Gray & Singer, 1987;Gray et al, 1989) The ERP frequency components (obtained by adaptive digital filtering) and also the amplitude frequency characteristics reflect a global and general frequency behavior (or frequency contents) of the compound potentials, which we call ERPs. As outlined by Başar (1980, chapters on the neural correlates of EEG and ERPs), the compound potentials and the filtered responses give only a general idea about the frequency distribution of the real neuronal activity.…”