The leading sense: supramodal control of neurophysiological context by attention

Abstract

Attending to a stimulus enhances its neuronal representation, even at the level of primary sensory cortex. Cross-modal modulation can similarly enhance a neuronal representation, and this process can also operate at the primary cortical level. Phase reset of ongoing neuronal oscillatory activity has been shown to be an important element of the underlying modulation of local cortical excitability in both cases. We investigated the influence of attention on oscillatory phase reset in primary auditory and visual cortices of macaques performing an intermodal selective attention task. In addition to responses "driven" by preferred modality stimuli, we noted that both preferred and nonpreferred modality stimuli could "modulate" local cortical excitability by phase reset of ongoing oscillatory activity, and that this effect was linked to their being attended. These findings outline a supramodal mechanism by which attention can control neurophysiological context, thus determining the representation of specific sensory content in primary sensory cortex.

Figure 1. Laminar CSD, CSD amplitude and ITC profiles of responses to preferred and non-preferred modality stimuli in A1 and V1

A) Field potentials (used to calculate the CSD) and MUA were recorded concomitantly with a linear-array multi-contact electrode positioned to sample from all cortical layers. Laminar boundaries were determined based on functional criteria. Color-maps on the left show the laminar profiles of representative attended standard auditory (preferred modality, upper) and attended standard visual (non-preferred modality, lower) stimulus related averaged CSD (236 and 253 sweeps respectively) recorded in the same A1 site. Current sinks (net inward transmembrane current) are red and current sources (net outward transmembrane current) are blue. Traces below show concomitantly recoded MUA averaged across all cortical layers. Color-maps in the middle are the laminar profiles of averaged and baseline corrected single trial CSD amplitudes on the same scale as the CSD maps to the left. Traces below are CSD amplitudes averaged across all layers. Color-maps on the right show the laminar profiles of auditory and visual stimulus related ITC averaged in the 4–100 Hz frequency range for each of the electrode channels. Traces below depict ITC from the supragranular channel where it was maximal related to non-preferred modality (in A1, visual) stimuli. Note that auditory and visual stimulus related ITC are mapped to different y axes located on the left and right respectively. B) The same electrophysiological variables are shown as in panel A) but in V1, in response to attended standard visual stimuli (upper) as preferred and attended standard auditory stimuli (lower) as non-preferred modality. C) & D) Responses are to the same stimuli in the same sites as A) & B) but from trial blocks when the stimuli were ignored.

Figure 2. Pooled ITC related to attended versus ignored stimuli in A1 and V1

A) Time-frequency plots show ITC values from selected supragranular electrode channels (see Supplemental Experimental Procedures) averaged across all A1 sites (n=19) related to attended and ignored auditory (upper) and visual (lower) stimuli. Contour plots demarcate regions of pooled ITC values that are significantly larger (at 95% 99% and 99.9% confidence levels) than the ITC value above which a significantly non-random phase distribution can be assumed (calculated using the Rayleigh statistic, p<0.01). Traces to the right display ITC values for frequencies between 4 and 100 Hz related to attended (light blue) and non-attended (dark blue) stimuli at the time of the maximal gamma ITC peak to attended stimuli marked by gray arrows (the exact latency is show for each ITC peak). Red lines on the frequency-axis denote frequency ranges where ITC related to attended stimuli is significantly greater than ITC related to ignored ones (dependent t-test, p<0.01, n=19). B) Same as in A) but pooled ITC values displayed are from supragranular V1 sites (n=25) related to attended and ignored visual (upper) and auditory (lower) stimuli.

Figure 3. Frequency and timing of maximal gamma and theta ITC related to attended auditory and visual stimuli

A) Box-plots show the pooled frequency of maximal ITC in the gamma (left) and theta (right) range related to attended stimuli in A1 (n=19) and V1 (n=25) (A1A - auditory stimuli, A1; A1V - visual stimuli, A1; V1V - visual stimuli, V1; V1A - auditory stimuli, V1). The boxes have lines at the lower quartile, median, and upper quartile values while the notches in boxes graphically show the 95% confidence interval about the median of each distribution. Brackets indicate the significant post hoc comparisons calculated using Tukey’s test (p<0.01). B) Pooled timing of maximal ITC in the gamma (continuous line, shorter latencies) and theta (dotted line, longer latencies) range related to attended stimuli from all experiments. As in A), brackets denote significant post hoc comparisons.

Figure 4. Pooled auditory and visual stimulus related mean gamma and theta phase

Histograms show the distribution of mean (across trials within each experiment) auditory (30 ms post-stimulus) and visual (50 ms post-stimulus) gamma and theta phases in A1 and V1. P-values were calculated using the Rayleigh test of uniformity.

Figure 5. Ongoing oscillatory activity in the supragranular layers of A1 and V1

A) Averaged spectrograms of ongoing activity from the supragranular layers of all A1 (magenta trace, n=19) and V1 (blue trace, n=25) sites. Before averaging, individual spectrograms were normalized to the average amplitude between 4 and 100 Hz. Horizontal lines denote the theta and gamma frequency ranges that were used to search for amplitude peaks in the spectrogram of each site. B) Pooled frequency of dominant gamma (upper) and theta (lower) activity in A1 and V1. Bracket indicates a significant difference calculated using independent two sample t-test (p<0.01).