Title: Mechanisms of attention in visual cortex and the amygdala
Description: Spatial attention enhances perception at specific locations in the visual field, measured behaviorally as improved task performance and faster reaction times. In visual cortex, neurons with receptive fields at attended locations display enhanced responses. This neural modulation is presumed to underlie the associated behavioral benefit, although the mechanisms linking sensory cortical modulation to perceptual enhancement remain unclear. In studies of spatial attention, experimentalists persuade animals to attend to particular locations by associating them with a higher probability or magnitude of reward. Notably, these manipulations alter in tandem both the absolute expectation of reward at a particular location, as well as the expectation of reward relative to other locations in the visual field. We reasoned that independently changing absolute and relative reward expectations could provide insight into the mechanisms of attention. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while independently varying the reward magnitude associated with correct discrimination at each location.

Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in visual area V4 were consistently modulated by absolute reward value, exhibiting increased firing rates, increased gamma-band power, and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. Thus, neural modulation in V4 can be robustly dissociated from the perceptual benefits of spatial attention; performance could be enhanced without neural modulation, and neural activity could be modulated without substantial perceptual improvement. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms. In identifying brain areas involved with attention, a distinction is generally made between sensory areas like V4— where the representation of the visual field is modulated by attentional state— and attentional “source" areas, primarily in the oculomotor system, that determine and control the locus of attention.

The amygdala, long recognized for its role in mediating emotional responses, may also play a role in the control of attention. The amygdala sends prominent feedback projections to visual cortex, and recent physiological studies demonstrate that amygdala neurons carry spatial signals sufficient to guide attention. To characterize the role of the amygdala in the control of attention, we recorded neural activity in the amygdala and V4 simultaneously during performance of the orientation discrimination task. In preliminary data analysis, we note two sets of findings. First, consistent with prior work, we found that amygdala neurons combine information about space and value. Rewards both contralateral and ipsilateral to amygdala neurons modulated responses, but contralateral rewards had a larger effect. Therefore, notably distinct from known attentional control sources in the oculomotor system, spatial-reward responses in the amygdala do not reflect the relative value of locations. Second, we found signatures of functional connectivity between the amygdala and V4 during task performance.

Reward cue presentation was associated with elevated alpha and beta coherence, and attention to locations contralateral to the amygdala and inside the receptive field of V4 neurons was associated with elevated inter-area gamma coherence. These results suggest that the amygdala may serve a unique role in the control of spatial attention. Together, these experiments contribute towards an understanding of the brain-to-behavior mechanisms linking neural activity in V4 and the amygdala to the dramatic perceptual and behavioral improvement associated with attention.