Learning Objectives
By the end of this section, you should be able to
- 19.5.1 Articulate the different neuropsychological conditions associated with impaired attentional operations, as well as the varieties of each.
- 19.5.2 Explain the relationship between ADHD and forms of attentional disruption that result from brain damage.
Much of our discussion thus far has focused on attentional function in the healthy, typically developing brain. There are, however, a number of neuropsychological and neurodevelopmental disorders that provide unique insights into the brain systems involved in attention. In this section, we'll review a few such disorders to see how they disrupt the normal operations of the attentional system, and how they inform our theories of attention in the healthy brain.
Neglect and extinction
One of the most striking disruptions of attentional function after brain damage is a condition known as spatial neglect (also commonly referred to as visual neglect, hemispatial neglect, or hemineglect). The key feature of patients with this disorder is an inability to attend, or orient, to information from one side of space (Halligan et al., 2003; Parton et al., 2004; Rafal, 1994). Typically, the impacted side of space is contralesional, which means that if the patient has damage to the right side of the brain, then the left (opposite side) of the world will be ignored. Information on the same side as the brain damage (ipsilesional) is often, though not always (Kim et al., 1999), spared. Neglect patients engage with the world seemingly unaware of the presence of information on the contralesional side. They fail to notice objects and people on that side. They might only shave or apply makeup to half of their face. They might even leave half of the food on their plate, or only dress half of their body.
Not all neglect patients experience their problems in the same way. We'll see later that they vary in kind, with different manifestations depending on the type of information that's ignored. But they also vary in degree, ranging from mild to severe. In its mildest form, neglect may manifest itself as extinction (Driver & Vuilleumier, 2001; Riddoch, 2010), which refers to a situation in which patients fail to attend to contralesional visual input, but only when simultaneous input is also present in the ipsilesional visual field. In other words, if you present an extinction patient with information on just one side (even the contralesional, or "bad", side), they will be aware of it, and respond to it. However, if you present them with information simultaneously on both sides (double simultaneous stimulation), then they will only be aware of the information presented ipsilesionally (i.e., the "good" side; see Methods: Lesions).
Clinical features of neglect and extinction
The hallmark symptom of neglect is a failure to attend, or orient, to contralesional information. Most often, this results from damage to the right side of the brain, which means that the left side of the world is typically impaired. Clinicians diagnose this disorder in a number of ways; often using relatively simple pen-and-paper tests, like those shown in Figure 19.14
For instance, if you ask a neglect patient to make a mark in the middle of a horizontal line (a line bisection task), they will place their mark too far to the ipsilesional (typically the right) side. They think that they have split the line in half, but in fact, they are unaware of the left-most part of the line, and so they fail to recognize the true midpoint. In a similar task, patients might look at a sheet of paper with a scatter of lines and be asked to make a mark through all the lines that they see (a line cancellation task). Similar to the line bisection task, patients will cross out most of the lines on the right side of the page but miss most, if not all, of the lines on the left side.
Another rather basic diagnostic test involves drawing (Figure 19.14). If you ask a typical neglect patient to copy a picture that's in front of them, or if you ask them to draw a picture from memory, they will either fail to include details from the left side of the image, or in some cases, they'll include all the details but misplace them on the right side. They recognize the objects, but they fail to notice, or be aware of, information on one side of the image.
You might think that these previous examples could be easily explained by a lower-level visual impairment. For instance, maybe the patients are blind to one side of the visual world (a condition known as hemianopia). This is not the case, however, as visual examinations demonstrate that neglect patients have preserved lower-level visual processing, and they even show activation in striate and extrastriate brain regions for the information that they fail to attend (Rees et al., 2000). In fact, hemianopic patients don't exhibit the problems that you see in Figure 19.14 because they know they have a visual impairment, and they adjust accordingly (e.g., by turning their head so that everything falls into their sighted regions). Patients with neglect lack that insight into their condition, a condition known as anosagnosia. That is, they not only miss out on half of the world, but they are unaware that they are missing anything.
Neglect typically results from unilateral damage to the posterior and inferior parietal cortices but can also occur after frontal or subcortical lesions (Figure 19.14; Mort et al., 2003). Damage to either side of the brain can produce neglect, although it is more common after right-sided brain damage (Bowen et al., 1999). Despite this variability, notice that these regions overlap considerably with the dorsal and ventral attentional networks reviewed in 19.2 How is Attention Implemented in the Brain?. In fact, a number of theorists have argued that neglect is best characterized by a disruption of these two key attentional control networks (Corbetta & Shulman, 2011).
Unconscious processing of neglected information
Patients with neglect are unaware of information presented on the contralesional side of space. But is it better to characterize their condition as a problem of conscious awareness, or a problem of perceptual processing? Another way to think about this is to consider neglect in light of our earlier review of early and late selection in 19.3 What Happens to Unattended Information?. Some evidence suggests that neglected information is subjected to a relatively high level of semantic processing (late selection). For instance, Marshall & Halligan (1988) asked a patient to look at two houses arranged vertically so that the left side of each house fell into the neglected side of space. The right half of each house was identical, but the left side of one of the houses appeared to be on fire. The patient failed to notice any differences between the two houses (because the important differences were on the neglected side of space), but when asked where she would like to live, she routinely selected the house that was not on fire (even though she could not articulate a reason)! This finding has not been consistently replicated (e.g., Bisiach & Rusconi, 1990), but other lines of research suggest that neglect and extinction patients process semantic-level information about sensory input that's ignored. For instance, Berti and Rizzolatti (1992) presented an extinction patient with a double simultaneous stimulation task in which the two objects belonged to the same semantic category but looked very different perceptually (two different cameras seen from different angles), or two objects that looked perceptually similar, but belonged to different semantic categories (a spoon and a key). The patient was able to correctly categorize whether the two belonged to the "same" or "different" categories, even though they were unaware of the object presented contralesionally in the first place.
Different manifestations of neglect
Earlier, we defined neglect as a failure to attend, or orient, to one side of space. That was a somewhat general definition of the condition, and it intentionally glossed over an important aspect that we haven't considered so far, namely, that we can carve up space in many different ways. For instance, we can talk about the left and the right side of the environment around us, but we can also talk about the left and right sides of individual objects in that environment. Similarly, we can talk about space in terms of the external perceptual world, or in terms of our own internal "mental" space. These two examples illustrate the complexity of defining the exact spatial nature of neglect and give a preview of some of the different manifestations of the disorder.
In a classic neuropsychological study, Bisiach and Luzzatti (1978) asked two neglect patients to form a mental picture of the central square in their hometown of Milan, Italy. In one case, they were asked to imagine that they were on the East side looking West and to name all of the buildings that they could see in their "mind's eye". In this case, they mostly named landmarks on the North side of the square (which corresponded to the right side of their mental image) and reported very few buildings on the South side. Interestingly, when they were asked to flip their point of view (i.e., imagine standing on the West side facing East), they did just the opposite. That is, they named mostly buildings from the South side of the square (which now lined up with the right side of their mental image) and very few buildings from the North side. This demonstrates that neglect not only occurs for the external perceptual world, but can also occur for our own internal mental representations of space (representational neglect). Perceptual and representational neglect typically co-occur (Bartolomeo, 2002), but each can occur without the other (Ortigue et al., 2006), a phenomenon in neuropsychology known as a double dissociation.
Neglect can also manifest itself in different spatial frames of reference. For instance, neglect can occur for relatively close (Halligan & Marshall, 1991) or far (Vuilleumeir et al., 1998) regions of space. It can also occur for the left and right side of individual objects, a phenomenon known as object-based neglect (Robertson, 2004; Figure 19.15). If you ask a patient with object-based neglect to circle all of the "A"s on a piece of paper where the letters are clustered into two groups or "objects", they might circle the "A"s from the right side of each cluster, rather than just the "A"s on the right side of the page. Similarly, if they are asked to copy a scene, they might draw objects from the whole picture, but leave out details from the left side of each element. Marshall & Halligan, (1993) demonstrated that when a patient attempted to copy a single potted plant containing two flowers, they only copied the right half of the plant. Interestingly, when the patient was shown the top half of the same picture presented in isolation (which created two separate flowers), they copied the right sides of each flower! The anatomical correlates of each of these subtypes are not fully understood, although there are ongoing efforts to understand the distinct neural systems that give rise to each manifestation (for a review, see Buxbaum, 2006).
Treatment options for neglect patients
Spatial neglect is relatively common after right hemisphere brain damage (upwards of 50%; Buxbaum, 2004), but spontaneously resolves in a portion of those cases (Farne et al., 2004). For many individuals, however, the symptoms persist indefinitely, which presents significant challenges for daily life. Researchers have explored a range of methods to reduce symptom severity ranging from modest behavioral interventions to drug therapies and brain stimulation (for recent reviews, see Luauté et al., 2006; Umeonwuka et al., 2022).
One intervention strategy involves the use of prism adaptation (PA; Rossetti et al., 1998; Figure 19.16), in which patients wear specially designed goggles that shift their visual input in one direction (typically, that makes neglected information on the left side appear farther to the right). Rossetti and colleagues showed that a brief period of PA training (roughly 5 minutes) resulted in reduced neglect severity on a range of behavioral tests (e.g., line cancellation) that lasted for several hours. A recent meta-analysis suggests that this relatively low-cost and non-invasive form of therapy yields substantial benefits (Chen et al., 2022).
Another promising, although more intense, therapeutic option for neglect is caloric vestibular stimulation (CVS). This process involves inserting cold or warm water into the ear, which produces rapid involuntary sideways eye movements known as nystagmus. If cold water is delivered to the left ear in a patient with right brain damage, then it will cause the eyes to drift towards the left ear (the neglected side) followed by rapid eye movements back to center. It only takes a few minutes but reduces neglect symptoms significantly for several days following the intervention (Rubens, 1985; Rode et al., 1992).
One final technique that has been used to treat spatial neglect is transcranial magnetic stimulation (TMS; Müri et al., 2013). TMS delivers electric currents that can either boost or suppress cortical excitability in specific brain regions using a coil located on the person's scalp (see Methods: rTMS). The rationale behind its application in neglect stems from an influential theory of attention developed by Kinsbourne (1987) known as the hemispheric rivalry hypothesis. According to the theory, each brain hemisphere competes to pull your attention to the contralateral side, and neglect results from an unfair playing field after damage to one hemisphere, resulting in attention being drawn disproportionately to the ipsilesional side by the intact hemisphere. If this theory is correct, then suppressing brain activity in the intact hemisphere might level the playing fields, which would restore the balance of attentional pulls to each side. Several lines of evidence support this model, for instance, Brighina and colleagues (2013; Figure 19.16) suppressed brain activity in the contralesional parietal cortex of several neglect patients over the course of two weeks and found that it reduced neglect symptoms significantly and that the effects lasted beyond the TMS regimen.
Spotlight on ADHD
Developmental Perspective: Disorders such as neglect and extinction result from trauma to the brain such as a stroke or tumor, but there are other neurological conditions that are relevant to our discussion of attention. In fact, one of the most common neurodevelopmental disorders is Attention Deficit Hyperactivity Disorder (ADHD), which affects approximately 10% of all children (Bitsko et al., 2022). The hallmark features of ADHD are hyperactivity, impulse control, and (as its name implies), difficulty paying attention. The neuroanatomy of ADHD is not fully understood, but studies show that children with ADHD have lower gray and white matter volume relative to neurotypical children, particularly in prefrontal regions of the brain, as well as structural differences in regions such as the caudate nucleus and cerebellum compared to children without ADHD (Bush, 2010; Shaw et al., 2006; Valera et al., 2007). Functional brain imaging studies complement these findings, showing that activity in several of the regions linked to ADHD (e.g., the caudate and ventral striatum) is reduced (Kappel et al., 2015; Lei et al., 2015). In addition, specific neurotransmitter systems are thought to be play a role in ADHD, including dopamine and norepinephrine. In fact, one of the most common forms of treatment for ADHD involves the drug methylphenidate (Ritalin), which blocks the reuptake of norepinephrine and dopamine (effectively increasing the amount of these neurotransmitters available). Drug therapies are not the only treatment options available, however. In fact, behavioral approaches such as exercise and play therapy might be just as effective as drugs in treating ADHD. Some researchers have argued that reduced play behavior increases the risk of developing ADHD (Siviy & Panksepp, 2011), and that play and exercise interventions significantly improve ADHD symptoms (Vysniauske et al., 2020). These studies highlight an important feature of ADHD, which is that the mechanisms responsible for the underlying processes may well change across the lifespan. Indeed, the fMRI studies mentioned above showed that striatal activity reductions were more pronounced in children with ADHD compared to adults with ADHD (Kappel et al., 2015; Lei et al., 2015). Similarly, ADHD medications such as methylphenidate differentially affect cortical function in juvenile vs. adult rats (van der Marel et al., 2014), highlighting the fact that developmental perspectives are critical for understanding this complex disorder. Finally, studies suggest that males are more likely to be diagnosed with ADHD than females (Mowlen et al., 2019), and that the primary symptoms experienced by males and females with ADHD can differ markedly (Gershon, 2020). It is therefore also important to incorporate biological sex differences into any meaningful discussion of the disorder.
The diagnostic criteria for ADHD (American Psychiatric Association, 2022) refers to concepts such as not following through on instructions, difficulties organizing tasks, and problems with waiting your turn or interrupting other people. Those might sound like problems related to paying attention. However, they are also distinct aspects of our ability to plan and execute behaviors in a way that allows us to achieve our goals, which, as we'll learn in the next section, constitute the cognitive processes associated with executive function. It is sometimes difficult to distinguish between the concepts of attention and executive function, and in the case of ADHD, many researchers would argue that the key symptoms might be more appropriately characterized as problems with executive function (Rubia, 2018). We'll unpack these related processes more in the next section.