Parietal control of attentional guidance: The significance of sensory, motivational and motor factors
Introduction
Judicious selection is at the heart of goal directed behavior. To select appropriately in a complex environment an intelligent agent (be it a person, a rat or a monkey), must solve two problems. First, the agent must identify the most relevant source of information from among many potential alternatives. Second, it must be able to focus on the relevant source and block out irrelevant distractions. In both intuitive and scientific terms, we think of the cognitive operations that allow such adaptive selection as falling into the broad realm of “attention”.
It is often claimed that attention is necessary for overcoming capacity limitations inherent in neural processing. Because the brain is “bombarded” with more sensory information than it can process in depth, the argument goes, attention is needed to prioritize and limit the amount of information that reaches higher processing stages at any one time. However, the need for selection remains even in simple environments that do not seriously tax capacity limitations. Even in such environments, we must decide which objects are helpful to us and which are not. The essence of attention is therefore the act of assigning credit, or identifying the sources of information that are most relevant in a given context. Generally this decision requires learning about the statistical contingencies between various objects, actions and outcomes. It follows that attention must be a dynamic selection mechanism that is exquisitely sensitive to immediate task demands.
Neurophysiological investigations in non-human primates have focused on three areas as being important for the control of attention: the frontal eye field in the frontal lobe, the superior colliculus in the midbrain, and the lateral intraparietal area (LIP) in the parietal cortex. In this review we describe the state of our knowledge about one node of this network, area LIP, which has been especially well investigated and provides an excellent model system for further inquiry into the mechanisms of attention. Investigations into LIP began with the somewhat naïve view that an area controlling attention must simply represent objects or locations that are attended at a given moment and respond relatively weakly to distractors. To a first approximation, this is indeed what is found in LIP. However, recent evidence shows that this “priority map” is more complex and in particular that it takes on a wide range of task-specific properties – i.e., it appears to be plastic and adaptable to task demands. The specific significance of these modulations is not fully understood. However, we suggest that these modulations represent teaching signals through which the brain learns to assign attentional priority to various stimuli based on their significance for a specific action or a specific outcome. We end by describing a computational model (Roelfsema & van Ooyen, 2005) that may be a good starting point for formalizing inquiry into the links between learning and attention.
Section snippets
General methods and behavioral tasks
Data were collected with standard behavioral and neurophysiological techniques as described previously (Balan and Gottlieb, 2006, Oristaglio et al., 2006). All methods were approved by the Animal Care and Use Committees of Columbia University and New York State Psychiatric Institute as complying with the guidelines within the Public Health Service Guide for the Care and Use of Laboratory Animals. During experimental sessions monkeys sat in a primate chair with their heads were fixed in the
Area LIP
In the rhesus monkey, where it has been most extensively characterized, the LIP occupies a small portion of the lateral bank of the intraparietal sulcus (Fig. 1). Although a homologue of LIP is thought to exist in human parietal cortex, no consensus yet exists about its location and functional profile. Anatomically, LIP is well situated to receive visual, motor, motivational and cognitive information. It has extensive anatomical connections with an oculomotor structure, the frontal eye field
Conclusions
“Every one knows what attention is,” famously wrote William James in Principles of Psychology in 1890. “It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought.” This is indeed a compelling intuition, and one which guided the first forays of neurophysiologists into the black box that controls attention. These forays to some extent confirmed our intuition. Neurons in LIP, as well as those in the
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2020, CortexCitation Excerpt :In addition to saliency signals, these regions also incorporate information about a stimulus’ “top-down” relevance. The integration of top-down and bottom-up signals has led to the characterization of LIP and related regions as priority maps from which attention is allocated based on a winner-take-all computation (Bisley & Goldberg, 2010; Bogler et al., 2011; Gottlieb, Balan, Oristaglio, & Suzuki, 2009; Pollmann et al., 2003). Taken together, these studies suggest that expectations alter distractor processing in visual cortex, and this change leads to less attentional capture; however, when early suppression does not occur (or fails), then information about the salient distractor is carried forward into parietal cortex, competes for processing, and requires reactive attentional control to reject (Geng, 2014; Marini, Demeter, Roberts, Chelazzi, & Woldorff, 2016; van Diepen, Miller, Mazaheri, & Geng, 2016).
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2018, NeuroscienceCitation Excerpt :The PPC is a classical association area, where information from various sensory modalities converges (Mountcastle et al., 1975; Olcese et al., 2013; Wilber et al., 2014; Licata et al., 2017; Zhuang et al., 2017). It receives neuromodulatory input of the basal forebrain cholinergic system (Broussard, 2012) and is integral to the fronto-parietal network from which cognitive demands emerge such as attention, evidence accumulation and decision making (Platt and Glimcher, 1999; Buschman and Miller, 2007; Andersen and Cui, 2009; Gottlieb et al., 2009; Hanks et al., 2015; Goard et al., 2016). Finally, PPC receives input from thalamic regions different from those projecting to sensory cortices, mainly from lateral dorsal, lateral posterior and posterior nuclei (Kolb and Walkey, 1987; Reep et al., 1994; Reep and Corwin, 2009).