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Top-down Modulation

Top-down modulation: The crossroads of attention and memory.
How we perceive our environment involves an integration of two distinct influences: externally- and internally-driven attention. Sensory input from our surroundings often demand our attention based on stimulus characteristics such as novelty or salience (bottom-up processing), but we are also capable of directing attention toward or away from encountered stimuli based on our goals (top-down modulation).

Attention and memory have traditionally been viewed as distinct processes and have been studied independently. However, attention is a gateway to memory in that attended stimuli are better remembered than those that are not the focus of our attention. Furthermore, selective attention is necessary to restrict the contents of capacity-limited memory by limiting interference from irrelevant information (1). By serving as a neural basis for selective attention, top-down modulation influences our effectiveness in maintaining information in mind for brief periods of time (working memory), as well as consolidating information for later recall or recognition (long-term memory). Thus, top-down modulation serves as a foundation for diverse cognitive processes, such as attention, working memory and long-term memory.

In addition to the influence that attention has on memory during encoding new information, there is yet another aspect of mechanistic overlap. The neural signature of attention, top-down modulation of neural activity in sensory cortices, has been described not only when stimuli are present in the environment (e.g., selective attention and memory encoding (2-5)), but also when stimuli are absent and sensory representations are generated internally (e.g., mental imagery, working memory maintenance & stimulus anticipation (6-9)). Thus, top-down modulatory mechanisms involved in perception and attention to encountered stimuli may be the same as those that underlie the generation of mental images when stimuli are not present, a process that is intimately associated with memory.

Top-down modulation: Enhancement and Suppression.
Top-down modulation is a bi-directional process in that it underlies our critical ability to both focus our attention on task-relevant stimuli and ignore irrelevant distractions. This involves both the enhancement and suppression of neural activity in sensory cortical regions depending on the relevance of the information to our goals (10, 11). By generating neural contrast via the enhancement and suppression of activity, top-down signals bias the likelihood of successful representation of relevant information. It is well documented that inhibitory and excitatory mechanisms are present throughout the nervous system (e.g., spinal reflexes, cerebellar outputs and basal ganglia movement control). It is thus not surprising that top-down modulation entails both enhancement and suppression to regulate the impact that perceived sensory stimuli have on neural activity. This provides a powerful contrast for sculpting neural processes that support all higher cognitive operations.

The physiological basis of top-down modulation relies on extensive evidence from single-unit physiology, functional neuroimaging and EEG, which reveals that measures of neural activity are augmented in specialized sensory cortical regions—the presumed sites of representation—when attention is directed toward a stimulus or stimulus attribute (5, 12-14), while reciprocal suppression of activity occurs in sensory regions that encode non-relevant stimuli (15, 16). An important question that has emerged is whether enhancement and suppression are mechanistically distinct processes or are different levels of the same process.

Top-down modulation: Neural networks.
Theories of brain organization focus on two distinct, but complementary principles: modularity—the existence of neuronal assemblies with intrinsic functional specialization and, connectivity—the integration of signals from distant brain regions resulting in organized behavior. While the modular model may be reasonable to describe basic features of primary cortices, it is insufficient to explain complex cognitive processes, which cannot be localized to isolated brain regions. In order to adequately explore the neural mechanisms involved in such processes and their changes with aging, we need to direct our experimental design and analyses to studying interactions between brain regions, or neural networks. The network approach is especially important for understanding top-down modulation, the very basis of which is communication between distributed regions.

It is widely believed that goal-directed activity modulation during visual processing is not an intrinsic property of the visual cortex, but is achieved via connections between control regions in the prefrontal cortex, the source of the modulatory signal, and the visual cortex, the site of modulation where visual information is represented (review; (18)). Tract-tracing studies in experimental animals offer a structural basis for this claim by revealing long range reciprocal connections between these regions (19-21). Several of these pathways have been described in humans by post-mortem dissection (22) and more recently using diffusion tensor magnetic resonance imaging (23). Additionally, there is accumulating neurophysiological data supporting goal-directed prefrontal involvement in top-down modulation of posterior sensory cortex activity (reviews; (18, 24, 25)).

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