Charles M. Gray

Stimulus-Dependent Neuronal Oscillations in Cat Visual Cortex: Inter-Columnar Interaction as Determined by Cross-Correlation Analysis.

We have demonstrated previously that neurons in cat striate cortex, in response to their preferred stimuli, exhibit oscillatory responses in a frequency range of 40–60 Hz. Recently, we obtained evidence that such oscillatory responses can synchronize across columns. We have now performed an extensive analysis of this phenomenon for both unit and field potential responses. In addition, we studied the stimulus conditions leading to intercolumnar synchronization. We recorded both multi‐unit activity and local field potentials from area 17 of adult cats with arrays of several electrodes. Interelectrode distances ranged from 0.4 to 12 mm. For all pairs of unit (n = 200) and field potential (n = 174) recordings, we computed auto‐ and cross‐correlation functions. The modulation of the correlograms was quantified by fitting a damped sine wave (Gabor) function to the data. Cross‐correlation analysis of the unit data revealed that in 90 out of 200 cases the recorded cells established a constant phase‐relationship of their oscillatory responses. This occurred, on average, with no phase difference. If the receptive fields were nonoverlapping, we observed a synchronization primarily between cells with similar orientation preferences. Cells with overlapping receptive fields also showed a high incidence of synchronization if their orientation preferences were different. In this latter group, synchronization occurred even in cases where the stimulus was optimal for only one of the recording sites. Under conditions of monocular instead of binocular stimulation the oscillatory modulation of the responses was attenuated, but the cross‐correlogram still indicated a significant interaction. Similar effects were seen with the application of stationary instead of moving stimuli. A synchronization of oscillatory field potential responses was observed in 136 out of 174 paired recordings. At all distances investigated, the probability of synchronization of field potential responses was independent of the orientation preferences of the cells. However, the strength of interaction decreased with increasing spatial separation. Control experiments showed that the synchronization of field potential responses was not due to volume conduction. The results demonstrate that oscillatory responses at separate cortical sites can transiently synchronize. The probability and strength of synchronization are dependent on the spatial separation of the recorded cells and their orientation preferences. In addition, the cross‐columnar synchronization is influenced by features of the visual stimulus. It is suggested that this synchronization provides a mechanism for the formation of neuronal assemblies in the visual cortex.

Stimulus-dependent neuronal oscillations in cat visual cortex: receptive field properties and feature dependence

Previously we have demonstrated that neurons in the striate cortex of lightly anaesthetized cats exhibit oscillatory responses at a frequency near 50 Hz in response to their preferred stimuli. Here we have used both single and multiple unit recording techniques to determine: (i) the receptive field properties and laminar distribution of cells exhibiting oscillatory responses; and (ii) the influence of changing stimulus properties on the temporal behaviour of the oscillatory responses. Oscillatory responses were detected and evaluated by computation of the autocorrelation function of the neuronal spike trains. We recorded oscillatory responses in 56% of the standard complex cells and in 12% and 11% of the simple and special complex cells. Cells exhibiting oscillatory responses were located primarily in supra‐ and infragranular layers. The oscillatory modulation amplitude of the autocorrelation function was enhanced by binocular stimulation (9 out of 16 cells) and reduced by combined stimulation with optimal and orthogonally orientated light bars (16 out of 21 cells). Changing stimulus orientation caused no change in the oscillation frequency of the sampled population of cells, while oscillation frequency increased monotonically with respect to stimulus velocity within the range of 1–12 degrees per second (10 out of 11 cells). The oscillatory modulation of the autocorrelation function increased as a function of stimulus length within the boundary of the cells receptive field (11 out of 11 cells). In 6 out of these 11 cells, the responses did not show an oscillatory modulation if elicited by small moving spots of light. Moving stimuli were much more effective in evoking oscillatory responses than were stationary stimuli (19 out of 20 cells). In no instance, using either stationary or moving stimuli, was the phase of the oscillatory response synchronized with the stimulus. These results demonstrate functional heterogeneity among cells within striate cortex based on their temporal firing patterns and provide evidence that the temporal pattern of oscillatory cellular activity is influenced by changes in stimulus properties.

Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties

Previously, we have demonstrated that a subpopulation of visual cortical neurons exhibit oscillatory responses to their preferred stimuli at a frequency near 50 Hz (Gray & Singer, 1989). These responses can selectively synchronize over large distances of cortex in a stimulus-specific manner (Gray et al., 1989; Engel et al., 1990 alpha). Here we report the results of a new analysis which reveals the fine temporal structure inherent in these interactions. We utilized pairs of recordings of the local field potential (LFP) activity from area 17 in the anesthetized cat which met two criteria. The LFP was correlated with the underlying unit activity at each site and the recording sites were at least 5 mm apart in cortex. A moving-window technique was applied to compute cross correlograms on 100-ms epochs of data repeated at intervals of 30 ms for a period of 3 s during each direction of stimulus movement. A statistical test was devised to determine the significance of detected correlations. In this way we were able to determine the magnitude, phase difference, frequency, and duration of correlated oscillations as a function of time. The results demonstrate that (1) the duration of synchrony is variable and lasts from 100-900 ms; (2) the phase differences between and the frequencies of synchronized responses are also variable within and between events and range from +3 to -3 ms and 40-60 Hz, respectively; and (3) multiple correlation events often occur within a single stimulus period. These results demonstrate a high degree of dynamic variability and a rapid onset and offset of synchrony among interacting populations of neurons which is consistent with the requirements of a mechanism for feature integration.

Heterogeneity in local distributions of orientation-selective neurons in the cat primary visual cortex.

We have employed the tetrode technique, which allows accurate discrimination of individual neuronal spike trains from multiunit recordings, in order to examine the variation of orientation selectivity among local groups of neurons. We recorded a total of 321 cells from 62 sites in area 17 of halothane-anesthetized cats; each site contained between three to ten neurons that were estimated to be less than 65 microns away from the tetrode tip. For each cell, we determined the orientation tuning in response to moving bars. Of the cells tested, 8.4% were unresponsive, 22.7% had no preferential response to any particular orientation, while 68.8% were tuned. The average difference in preferred orientation between cell pairs recorded at the same site was 10.7 deg, but the variance in preferred orientation differences differed significantly among sites. Some clusters of cells exhibited the same or nearly the same orientation preference, while others had orientation preferences that differed by as much as 90 deg. Our data demonstrate that the tuning for orientation is more heterogeneously distributed at a local level than previous studies have suggested.

Mechanisms Underlying the Generation of Neuronal Oscillations in Cat Visual Cortex

Place an electrode on the surface or in the depth of nearly any neuronal structure in the brain of either vertebrates or invertebrates. Record the fluctuations of voltage produced by the flow of current, and what you are likely to observe is an irregular sequence of rhythmic changes of potential having a multitude of frequencies (Bullock and Basar, 1988). If your electrode happens to be within one of many structures responsive to sensory stimuli, the presentation of a stimulus will in many cases evoke a sustained rhythmic fluctuation of potential outlasting the stimulus. This propensity for neural structures to generate oscillatory waves of activity has come to be termed an “induced rhythm”. It is a general property of sensory as well as many other neuronal networks that is expressed during periods of activation. In this chapter we describe some of our recent observations of induced rhythms in the mammalian visual cortex and discuss the evidence for several neuronal mechanisms thought to underlie their generation.

Synchronization of Oscillatory Responses in Visual Cortex: A Plausible Mechanism for Scene Segmentation

Subjectively, it appears to us that the main function of our visual sense is to identify objects and to evaluate relationships between them. Unless we are confronted with specially designed perceptual tasks we tend to be unaware that the segmentation of the visual world into distinct objects and shapes is, by itself, a major achievement of our visual system. The retinal image of a visual scene consists of a two-dimensional, continuous distribution of grey levels. Before the visual system can identify particular figures or objects it needs to determine which of the various luminance values belong to individual objects, or the embedding background. Some grouping has to be performed in order to associate these luminance distributions with contours, to associate particular contours with a single object, and to segregate objects with overlapping contours from each other and from the background. These operations are commonly defined as scene segmentation or figure-ground segregation. Because they are usually carried out subconsciously and do not require the direction of selective attention to particular features of the scene these operations are commonly called “preattentive visual processes” or “early visual processes” (for review and examples see: 30,31,25,4,41,42,34).

Dynamics of Stimulus-Evoked Spike Timing Correlations in the Cat Lateral Geniculate Nucleus

Precisely synchronized neuronal activity has been commonly observed in the mammalian visual pathway. Spike timing correlations in the lateral geniculate nucleus (LGN) often take the form of phase synchronized oscillations in the high gamma frequency range. To study the relations between oscillatory activity, synchrony, and their time-dependent properties, we recorded activity from multiple single units in the cat LGN under stimulation by stationary spots of light. Autocorrelation analysis showed that approximately one third of the cells exhibited oscillatory firing with a mean frequency ∼80 Hz. Cross-correlation analysis showed that 30% of unit pairs showed significant synchronization, and 61% of these pairs consisted of synchronous oscillations. Cross-correlation analysis assumes that synchronous firing is stationary and maintained throughout the period of stimulation. We tested this assumption by applying unitary events analysis (UEA). We found that UEA was more sensitive to weak and transient synchrony than cross-correlation analysis and detected a higher incidence (49% of cell pairs) of significant synchrony (unitary events). In many unit pairs, the unitary events were optimally characterized at a bin width of 1 ms, indicating that neural synchrony has a high degree of temporal precision. We also found that approximately one half of the unit pairs showed nonstationary changes in synchrony that could not be predicted by the modulation of firing rates. Population statistics showed that the onset of synchrony between LGN cells occurred significantly later than that observed between retinal afferents and LGN cells. The synchrony detected among unit pairs recorded on separate tetrodes tended to be more transient and have a later onset than that observed between adjacent units. These findings show that stimulus-evoked synchronous activity within the LGN is often rhythmic, highly nonstationary, and modulated by endogenous processes that are not tightly correlated with firing rate.

1703 Statistical analysis of oscillatory neuronal activities in cat lateral geniculate nucleus

1703 STATISTICAL ANALYSIS OF OSCILLATORY NEURONAL ACTIVITIES IN CAT LATERAL GENICULATE NUCLEUS. HIROYUKI ITO. CHARLES M. GRAY, PEDRO MALDONADO. DeDt. of Enaineerinas, Kvoto Sanqvo Univ., . . Pvoto 60t JAPAN, Center for Neurohence, Univ. of CallfPrnla, Davis, USA, A large fraction of cell in the visual cortex of the cat display stimulus dependent, 30-60 Hz, oscillatory firing patterns that are often synchronous over a range of spatial scales. Many studies have been carried out to test the hypothesis that those oscillations result fromintracorticalnetwork and play a functional role invisualinformationprocessing. Ontheotherhand, spontaneous andstimulus-evokedrhythmicactivity also occurs in the lateral geniculate nucleus (LGN). It has been hypothesized that cortical oscillatory activity may be an epiphenomenon of the spontaneous activity in the LGN that originates in the retina. To further test this notion, we have recorded spontaneous and visually-evoked activity in the LGN of anesthetized cats andevaluated the spike trains using correlation and spectral analyses. Our conclusion is the following. A: There are at least two types of oscillatory activities in the LGN. One is spontaneous oscillation that is suppressedbythe visual stimulation and possibly originates in the retina. The other is stimulusinducedoscillationthat is stimulusdependent. B: Therearesynchronousoscillatoryactivities betweenboththelocalsites andthedistantsites (500micronseparation).C: Weconcludethattheoscillatory activities observedinthe LGNareNOTlikelyto causethose observedinthe cortex, because: 1) The frequency ranges are significantly different, 60-90 Hz in the LGN and 30-60 Hz in the cortex. 2) The oscillatory activity observedinthe LGN is highly stable. This contrasts with highly transient nature of the cortical oscillation. 3) The vigorous , stable, spontaneous oscillatoryactivity observedinthe LGNis not observed in the cortex.