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Review
. 2011 Dec;15(12):585-91.
doi: 10.1016/j.tics.2011.10.006. Epub 2011 Nov 8.

The role of neuromodulators in selective attention

Affiliations
Review

The role of neuromodulators in selective attention

Behrad Noudoost et al. Trends Cogn Sci. 2011 Dec.

Abstract

Several classes of neurotransmitters exert modulatory effects on a broad and diverse population of neurons throughout the brain. Some of these neuromodulators, especially acetylcholine and dopamine, have long been implicated in the neural control of selective attention. We review recent evidence and evolving ideas about the importance of these neuromodulatory systems in attention, particularly visual selective attention. We conclude that, although our understanding of their role in the neural circuitry of selective attention remains rudimentary, recent research has begun to suggest unique contributions of neuromodulators to different forms of attention, such as bottom-up and top-down attention.

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Figures

Figure 1
Figure 1
Cholinergic involvement in attentional selection. (a) Enhancement of attention effects in macaque V1 by Ach. The cartoon above depicts the behavioral task in which attention was directed covertly to a neuron’s RF stimulus (red spotlight) or to a stimulus outside of the RF (not shown) during fixation of a central spot (gray lines). The effect of spatial attention on the responses of V1 neurons to visual stimuli is quantified with a modulation index for stimuli of varying lengths. Positive indices indicate greater responses when attention is directed toward the stimulus within the neuron’s RF compared to when attention is elsewhere. Indices measured during control trials (red) and during iontophoretic application of acetylcholine (black) are shown. Adapted from [36]. (b) Cholinergic neurons in the owl’s IPC nucleus signal the physical salience of stimuli by a characteristic switch-response. The exemplar neuron responds almost invariantly to RF stimuli across a range of stimulus intensities as long as the stimulus is more physically salient than the other stimulus on the screen (distracter). When the RF stimulus is less salient, the neuron responds at a uniformly low rate. Salience is manipulated by varying the speed at which a given stimulus looms (target salience in this example is set at 7 degrees/second). IPC neurons were recorded in owls during passive viewing. Adapted from [46].
Figure 2
Figure 2
Dopamine-mediated FEF control of saccadic target selection and visual cortical processing. (a) Local manipulation of D1R-mediated activity within the FEF during single neuron electrophysiology in area V4. Lateral view of the macaque brain depicts the location of a recording microinjectrode within the FEF and of recording sites within area V4. Bottom diagram shows saccades evoked via electrical microstimulation at the infusion site (red traces) and the RF (green ellipse) of a recorded V4 neuron in an example experiment. (b) Free-choice saccade task used to measure the monkey’s tendency to make saccades to a target within the FEF RF vs. one at an opposite location. In the task, two targets appear at varying temporal onset asynchronies. The RF target can appear earlier or later than a target outside of the RF. The monkey’s bias toward either target is measured as the asynchrony at which the monkey chooses the target with equal probability. The bottom plot shows the leftward shift in the asynchrony curve (indicating more RF choices), following manipulation of D1R mediated FEF activity. (c) Visual responses of a V4 neuron with a RF that overlapped the FEF RF measured during passive fixation. The plot shows mean ± standard error of the mean (SEM) visual responses to bar stimuli presented at varying orientations and the baseline firing rate in the absence of visual stimulation (dashed lines) before (black) and after (red) the FEF D1R manipulation. Adapted from [58].
Figure 3
Figure 3
Possible influence of D1Rs on recurrent networks within the PFC (specifically FEF) and between the PFC and V4. The diagram depicts two adjacent FEF or V4 columns representing different, but adjacent, locations in saccadic or visual space, respectively. The columns are assumed to interact competitively (black inhibitory neurons). Positive arrows between FEF neurons within the same column depict the recurrent excitatory connections thought to underlie the persistence of spatial signals during remembered saccades or locations. Recurrence between the FEF and V4 is proposed to underlie the influence of FEF on the gain of visual inputs within V4. Dopaminergic input from the ventral tegmental area (VTA, input at right) to the PFC may modulate recurrence both within the FEF and between FEF and V4 through D1Rs and to influence competition between spatial representations. For example, increases in recurrence in a particular column while remembering or attending to a corresponding location (thicker arrows at left) can be modulated by the level of dopamine. Biases in competitive interactions between columns within visual cortex can also be achieved by experimental manipulation of D1R-mediated FEF activity, as the results of [58] suggest. Also shown are the projections from infragranular FEF neurons to the superior colliculus (SC). Other anatomical details are omitted for simplicity. Red circles represent D1Rs and blue circles D2Rs. Note the localization of D2Rs primarily in infragranular, SC-projecting layers [50,55] which is consistent with the observation that changes in D2R-mediated FEF activity only affects target selection, and not visual cortical activity [58]. The inset at the upper right depicts the involvement of DA inputs in ‘synaptic triads’, in which those inputs coincide with glutamatergic (AA) ones [52].

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