Nonlinear changes in pupillary attentional orienting responses across the lifespan.

The cognitive aging process is not necessarily linear. Central task-evoked pupillary responses, representing a brainstem-pupil relationship, may vary across the lifespan. Thus we examined, in 75 adults ranging in age from 19 to 86, whether task-evoked pupillary responses to an attention task may serve in as an index of cognitive aging. This is because the locus coeruleus (LC), located in the brainstem, is not only among the earliest sites of degeneration in pathological aging, but also supports both attentional and pupillary behaviors. We assessed brief, task-evoked phasic attentional orienting to behaviorally relevant and irrelevant auditory tones, stimuli known specifically to recruit the LC in the brainstem and evoke pupillary responses. Due to potential nonlinear changes across the lifespan, we used a novel data-driven analysis on 6 dynamic pupillary behaviors on 10% of the data to reveal cut off points that best characterized the three age bands: young (19-41 years old), middle aged (42-68 years old), and older adults (69 + years old). Follow-up analyses on independent data, the remaining 90%, revealed age-related changes such as monotonic decreases in tonic pupillary diameter and dynamic range, along with curvilinear phasic pupillary responses to the behaviorally relevant target events, increasing in the middle-aged group and then decreasing in the older group. Additionally, the older group showed decreased differentiation of pupillary responses between target and distractor events. This pattern is consistent with potential compensatory LC activity in midlife that is diminished in old age, resulting in decreased adaptive gain. Beyond regulating responses to light, pupillary dynamics reveal a nonlinear capacity for neurally mediated gain across the lifespan, thus providing evidence in support of the LC adaptive gain hypothesis.

Grounding the Attentional Boost Effect in Events and the Efficient Brain.

Attention and memory for everyday experiences vary over time, wherein some moments are better attended and subsequently better remembered than others. These effects have been demonstrated in naturalistic viewing tasks with complex and relatively uncontrolled stimuli, as well as in more controlled laboratory tasks with simpler stimuli. For example, in the attentional boost effect (ABE), participants perform two tasks at once: memorizing a series of briefly presented stimuli (e.g., pictures of outdoor scenes) for a later memory test, and responding to other concurrently presented cues that meet pre-defined criteria (e.g., participants press a button for a blue target square and do nothing for a red distractor square). However, rather than increasing dual-task interference, attending to a target cue boosts, rather than impairs, subsequent memory for concurrently presented information. In this review we describe current data on the extent and limitations of the attentional boost effect and whether it may be related to activity in the locus coeruleus neuromodulatory system. We suggest that insight into the mechanisms that produce the attentional boost effect may be found in recent advances in the locus coeruleus literature and from understanding of how the neurocognitive system handles stability and change in everyday events. We consequently propose updates to an early account of the attentional boost effect, the dual-task interaction model, to better ground it in what is currently known about event cognition and the role that the LC plays in regulating brain states.

Auditory Target Detection Enhances Visual Processing and Hippocampal Functional Connectivity.

Though dividing one's attention between two input streams typically impairs performance, detecting a behaviorally relevant stimulus can sometimes enhance the encoding of unrelated information presented at the same time. Previous research has shown that selection of this kind boosts visual cortical activity and memory for concurrent items. An important unanswered question is whether such effects are reflected in processing quality and functional connectivity in visual regions and in the hippocampus. In this fMRI study, participants were asked to memorize a stream of naturalistic images and press a button only when they heard a predefined target tone (400 or 1,200 Hz, counterbalanced). Images could be presented with a target tone, with a distractor tone, or without a tone. Auditory target detection increased activity throughout the ventral visual cortex but lowered it in the hippocampus. Enhancements in functional connectivity between the ventral visual cortex and the hippocampus were also observed following auditory targets. Multi-voxel pattern classification of image category was more accurate on target tone trials than on distractor and no tone trials in the fusiform gyrus and parahippocampal gyrus. This effect was stronger in visual cortical clusters whose activity was more correlated with the hippocampus on target tone than on distractor tone trials. In agreement with accounts suggesting that subcortical noradrenergic influences play a role in the attentional boost effect, auditory target detection also caused an increase in locus coeruleus activity and phasic pupil responses. These findings outline a network of cortical and subcortical regions that are involved in the selection and processing of information presented at behaviorally relevant moments.

Estimates of locus coeruleus function with functional magnetic resonance imaging are influenced by localization approaches and the use of multi-echo data.

The locus coeruleus (LC) plays a central role in regulating human cognition, arousal, and autonomic states. Efforts to characterize the LC's function in humans using functional magnetic resonance imaging have been hampered by its small size and location near a large source of noise, the fourth ventricle. We tested whether the ability to characterize LC function is improved by employing neuromelanin-T1 weighted images (nmT1) for LC localization and multi-echo functional magnetic resonance imaging (ME-fMRI) for estimating intrinsic functional connectivity (iFC). Analyses indicated that, relative to a probabilistic atlas, utilizing nmT1 images to individually localize the LC increases the specificity of seed time series and clusters in the iFC maps. When combined with independent components analysis (ME-ICA), ME-fMRI data provided significant improvements in the temporal signal to noise ratio and DVARS relative to denoised single echo data (1E-fMRI). The effects of acquiring nmT1 images and ME-fMRI data did not appear to only reflect increases in power: iFC maps for each approach overlapped only moderately. This is consistent with findings that ME-fMRI offers substantial advantages over 1E-fMRI acquisition and denoising. It also suggests that individually identifying LC with nmT1 scans is likely to reduce the influence of other nearby brainstem regions on estimates of LC function.

Attending to behaviorally relevant moments enhances incidental relational memory.

Memory for the items one has recently encountered is sometimes enhanced in divided attention tasks: Attending to behaviorally relevant items, such as a target in a detection task, boosts memory for unrelated background items (e.g., scenes or words). However, a central feature of episodic memory is memory for the spatiotemporal relationship between items and other elements of an event (relational memory), not just the item itself. Three experiments examined whether attending to a behaviorally relevant target-item boosts memory for the relationship between that item, its features, and a background scene. Participants memorized briefly presented scenes. At the same time, they pressed a button if a second unrelated item (a figure or face) was a particular target color (Experiments 1 and 2) or target gender (Experiment 3) rather than a distractor color or gender. Target and distractor items also varied in task-irrelevant features (shape, location, or facial identity). If attending to behaviorally relevant events influences relational memory, then participants should be better able to report both target-defining and irrelevant features of items that appeared with target-paired scenes rather than distractor-paired scenes. This was the case in all experiments: memory was enhanced for the target-paired scenes as well as the association between a scene and features of the paired target-item. Attending to behaviorally relevant moments therefore has broader effects on memory encoding than previously thought. In addition to boosting memory for unrelated background items, attending to targets facilitates relational memory in these tasks.