Attention-related changes in correlated neuronal activity arise from normalization mechanisms

Abstract

Attention is believed to enhance perception by altering the activity-level correlations between pairs of neurons. How attention changes neuronal activity correlations is unknown. Using multielectrodes in monkey visual cortex, we measured spike-count correlations when single or multiple stimuli were presented and when stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, nonpreferred stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly tuned neurons but decreased spike-count correlations between pairs of oppositely tuned neurons. A stochastic normalization model containing populations of oppositely tuned, mutually suppressive neurons explains these changes and also explains why attention decreased or increased correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms.

Figure 1. Multi-electrode array recordings of neuronal activity in area V4 during a visual attention task

a, Simultaneous recordings of the responses of multiple neurons in area V4 of rhesus monkeys. b, In separate blocks of trials, monkeys attended to one of four stimulus locations, either near the RFs of the recorded V4 neurons (location 1 and 2) or far from the RFs (location 3 and 4). The central white dot represents the fixation point on the display. c, Each of the two RF stimuli evokes excitation, which increases responses, and suppression, which decreases responses. Normalization mechanisms determine how neurons combine the suppressive and excitatory contribution of each stimulus into a response. By fitting a normalization model to the observed neuronal responses in all conditions, the excitatory and suppressive contribution of each stimulus were estimated.

Figure 2. Normalization mechanisms determine spike-count correlations

All data in these plots were obtained while monkeys' attention was directed far from the RF stimuli (locations 3, 4 Figure 1b). a, Each neuron's preferred stimulus in a stimulus pair was the stimulus that contributed most excitation (blue arrows). Positive selectivity indices refer to neuron pairs with the same stimulus preference (blue arrows upper half plot). Negative selectivity indices refer to neuron pairs with opposite stimulus preferences (blue arrows lower half plot). Values of non-preferred suppression near zero indicate that the two neurons of a neuron pair were weakly suppressed by their non-preferred stimulus (thin orange dashed line left side plot), values near one indicate strong suppression by their non-preferred stimulus (thick orange dashed line right side plot). For neurons with opposite selectivity (lower half plot), the preferred stimulus of one neuron is the non-preferred stimulus of the other neuron. b, Mean spike-count correlations, indicated by color, as a function of the selectivity and non-preferred suppression of neuron pairs, measured while a single stimulus was presented alone near the RF. c, Mean spike-count correlations during paired stimulus presentations. d, Difference in spike-count correlations between c and b. Plots based on regularized bilinear interpolation (Online Methods). e, Mean spike-count correlations (r_sc) computed on the data from four quadrants in the space spanned by selectivity and non-preferred suppression (quadrants defined as a combination of negative or positive selectivity, and non-preferred suppression < 0.5 or > 0.5). Black: paired stimulus presentations. Gray: Single stimulus presentations. Error-bars represent ± 1 SEM. f, Pattern of spike-count correlations can be explained by two oppositely-tuned neuronal populations, Population A and B, that mutually suppress each other's activity. Common suppression, evoked by neurons in Population B, correlates the activity of neuron 1 and 2 in Population A, but decorrelates the activity of neurons in different populations, e.g. neuron 1 and 3.

Figure 3. Visual attention engages normalization mechanisms to modulate spike-count correlations

All data in these plots were obtained during paired stimulus presentations with attention directed to one of two RF stimuli (locations 1, 2 Figure 1b). Data are shown for neuron pairs with the same selectivity (selectivity > 0; see Figure 4 for opposite selectivity). a, Spike-count correlations decrease when the preferred stimulus is attended relative to when attention is directed far from the RF stimuli. b, Spike-count correlations increase when the non-preferred stimulus is attended relative to when attention is directed far from the RF stimuli. c, Attention modulation of spike-count correlations: comparing a and b. d, Mean spike-count correlations (r_sc) computed on the data from four quadrants in the space spanned by selectivity and non-preferred suppression in a, b and c (quadrants defined by a combination of selectivity < 0.5 or > 0.5 and non-preferred suppression < 0.5 or > 0.5). Black: attention directed far from the RF stimuli. Blue: attention directed to the preferred stimulus of neuron pairs. Orange: attention directed to the non-preferred stimulus of neuron pairs. Error-bars represent ± 1 SEM. e, Attending the preferred stimulus of neurons in Population A increases neuronal activity in Population A (thick circles), which increases suppression to neurons in Population B (thick orange line). The less active neurons in Populations B (thin circles) send less common suppression to neurons in Population B (thin orange line), thereby decorrelating activity in Population A. f, Attending the preferred stimulus of neurons in Population B increases neuronal activity within Population B, which increases common suppression to neurons in Population A, thereby correlating activity in Population A.

Figure 4. Little attention modulation of spike-count correlations for neuron pairs with opposite selectivity

For oppositely-tuned neuron pairs (selectivity < 0), attend preferred and non-preferred are not defined: one neuron's preferred stimulus is the other neuron's non-preferred stimulus. So we compared conditions in which attention was directed far from the RF stimuli to conditions in which attention was directed toward one of two RF stimuli. a, Attention modulation of spike-count correlations. b, Mean spike-count correlations computed on the data from four quadrants in the space spanned by selectivity and non-preferred suppression indices in a. Black: paired stimulus presentations with attention directed far from the RF stimuli. Brown: spike-count correlations with attention directed toward one of two RF stimuli. Error-bars represent ± 1 SEM. c, Correlations between neurons in Population A and neurons in Population B (e.g. neurons 1 and 3) change little compared to the condition with attention directed Far from the RF, because increased suppression in one direction is canceled by decreased suppression in the other direction.

Figure 5. A stochastic normalization model accounts for the main trends in the observed correlations

The model is based on two mutually-suppressive neuronal populations with opposite stimulus preferences. a, Model output for the conditions with attention directed far from the RF stimuli. Conventions as in Figure 2d. b, Model output for the conditions with attention directed to the preferred stimulus of similarly-tuned neuron pairs. Conventions as in Figure 3a. c, Model output for the conditions with attention directed to the non-preferred stimulus of neuron pairs with similar stimulus selectivity. Conventions as in Figure 3b. d, Model output for the conditions with attention directed to one of two receptive field stimuli for neuron pairs with opposite stimulus selectivity. Conventions as in Figure 4a.

Figure 6. Normalization mechanisms affect spike-count correlations similarly for stimuli inside the classical receptive field or in the surround

Left column, stimulus configurations with two stimuli inside the cRF. Right column, stimulus configurations with one stimulus inside the cRF and one stimulus inside the surround. a and b, Same conventions as in Figure 2d. Note the different scale bars between a and b. c and d, Same conventions as in Figure 3a. e and f, Same conventions as in Figure 3b.