Chapter 10 – Attention

Definitions

Attention is the selecting of specific information for further processing. It can be divided into 4
categories. Alertness and arousal are necessary to establish attention. Vigilance is sustained
attention. Selective attention is the selection of information essential to a task and consists mostly of
a filtering process. Divided attention is what we know as “multitasking” – splitting attention across
tasks. Multiple-resource theory suggests a limited set of distinct resource pools (type-specific, i.e.
“verbal” vs. “spatial” resources).

1. Brain structures mediating arousal

At the most basic level, the ability to pay attention requires the nervous system to be receptive to
stimulation. The brain system responsible for overall arousal is the ascending reticular activating
system (RAS). Not surprisingly, this system is also responsible for controlling sleep–wake cycles. The
RAS is so critical to alertness that coma results when it is damaged (bilateral lesions) or disrupted
(because of meningitis, trauma, toxins etc.).

The cell bodies of the ascending RAS are located in the brainstem and connect diffusely to most
regions of the cortex, allowing it to modulate the arousal of the entire cortex via two routes: a dorsal
system that travels to the cortex via the thalamus (mainly ACh), and a ventral route that travels to
the basal forebrain and subsequently onto the cortex (Serotonin, NA).

The thalamus, to which the dorsal brainstem nuclei project, uses glutamate (main excitatory
neurotransmitter in the brain) to modulate the level of arousal of the cortex. The portions of the
thalamus that are specifically implicated in this function are the medial dorsal, intralaminar, and
reticular nuclei. Damage restricted to these thalamic nuclei is enough to result in coma, while electric
stimulation can increase responsiveness to commands and the ability to control the limbs in patients
in a minimally conscious state.

The ventral route involves two major neurotransmitter systems: the noradrenergic system and the
serotonergic system. The cell bodies of the noradrenergic system are located within the locus
coeruleus of the brainstem. Single-cell recordings reveal that cells in the locus coeruleus fire at a
regular slow rate (about 1 Hz), but increase their firing in response to arousing stimuli and decrease
their firing during periods of drowsiness and sleep. In fact, activity in the locus coeruleus appears to
prevent sleep. The noradrenergic system appears to be involved in stress-related aspects of arousal
and has been implicated in psychiatric disorders, such as posttraumatic stress syndrome, that are
characterized by hyperaroused states.

The other major neurotransmitter involved in arousal is serotonin (5-HT). The cell bodies for this
subsystem are located in the raphe nucleus. This subsystem is proposed to be involved in arousal by
aiding in wakefulness and suppressing rapid eye movement (REM) sleep. Activity of these cells
increases during wakefulness and decreases substantially or almost ceases during REM sleep.
2. Brain structures mediating vigilance (sustained attention)

The cholinergic system and the noradrenergic system – as described in the section about arousal –
also play a role in vigilance and sustained attention. The noradrenergic system appears to be
important for alerting the brain that it should get ready to receive information or make a response
(arousal). It also helps to sustain a constant attentive state via a constant, tonic level of arousal. The
thalamus may act as an interface between “bottom-up” arousal and “top-down” vigilance.

Furthermore, electrophysiological recordings suggest a right lateralized system for sustained

attention. For example, although brain damage almost always slows responses to stimuli, damage to
the right hemisphere causes the greatest decrement in performance, regardless of whether stimuli
are auditory or visual and heart-rate responses to warning signals are also disrupted by right-
hemisphere damage.

3. Selective attention

Selective attention - prioritizing certain pieces of information for processing over others – is probably
the most studied aspect of attention. In bottom-up attentional selection, some intrinsic aspect of the
stimulus itself causes it to be attended, that is, to receive priority in processing (i.e. salience). In
contrast, in top-down attentional selection, the person determines how to direct his or her attention
according to any number of different features.

The time course of attentional selection

Rather than thinking of attention as a single filter, it is better to think of it as a series of filters that act
during different time frames of stimulus processing. Thanks to ERPs, it is clear nowadays, that instead
of only early-selection (attentional selection occurs before items are identified) or only late-selection
(selection occurs only after sensory processing is complete and items have been identified and
categorized), selection happens at multiple times in processing.

At approximately 80ms after stimulus presentation, there is an increased negative shift for the
attended stimulus (compared to an unattended stimulus), which is often called the Nd (negative
difference) component. It describes an advantage in processing when attention was shifted towards
this stimulus beforehand.

The N2pc component, which occurs approximately 180–280 ms after stimulus presentation, is
thought to reflect the focusing of attention on potential target items in a display in order to prioritize
processing of these items over distractors. (It is labelled “pc” because it is recorded maximally over
parietal areas contralateral to the position of the target.) The P300 (which occurs at least 300 ms
post-presentation) is found only when a person is paying attention and monitoring the sensory world
for a task-relevant target.

Brain regions involved in selective attention

a) Superior Colliculus: Automatic Orienting = Moving the focus

The superior colliculus controls eye movements (=saccades) – even though attention must not always
be where you look at (=covert attention). Express saccades, which take about 120ms, tend to be
reflexive and are triggered by the appearance of a novel visual stimulus in the periphery. Regular
saccades, about 200 to 300ms, can be driven by the saliency of external stimuli or under voluntary
control.

The superior colliculus is divided into 3 distinct layers. The first, the superficial layer, contains
neurons that respond quickly to temporal and spatial features of visual stimuli, and has a retinotopic
map. The other two layers, the intermediate and deep layers, contain neurons that are sensitive both
to sensory characteristics and to orienting movements. These layers are organized in an oculocentric
manner with regards to where the eyes will move. These portions of the superior colliculus are
tightly coupled to the oculomotor regions of the brainstem that serve as the final common pathway
for control of eye movements.

It has also been connected to directing attention in the auditory modality or crossmodal tasks, such
as looking at lips while listening.

b) Thalamus: gating of sensory information

The lateral geniculate is the thalamic relay point for input received from the eyes, enhancing relevant
information and suppressing irrelevant information depending on the focus of attention
(=”gatekeeper”). The pulvinar appears to aid in regulating information transmission between cortical
regions (=”mediator”) and synchronizing them.

c) Parietal lobe

Most important for distributing attentional resources, but also processing of attention overall (i.e.
lesions can result in hemineglect syndrome, where one visual field is not attended). The main
streams of information here consist of top-down directing, bottom-up reorienting and their
integration to form prioritizations of information.

Top-down selection happens mostly in the superior PL: attention must be disengaged from the
current location of attention and then it
must be shifted to a new location.
Bottom-up salience is controlled by the
inferior PL, detecting unattended or low-
frequency events. The intraparietal sulcus
has been connected to priority maps.
Feature integration theory postulates that
attention is needed to combine features
(such as colour and shape in a visual
search task). While single features can be
more or less salient, there are influences
of top-down processes on this priority
map. Exemplary task: Look for a small
black box.

Anterior cingulate and supplementary motor area help in the response-related selection by choosing
specific content from attended material (e.g. the correct naming of the colour in a Stroop task).
There are different brain regions involved with selection among competing responses for specific
modalities – manual movements differ from saccades, for example.
Finally, the lateral prefrontal cortex is an important instance for top-down goal selection and is often
referred to as an executive function.

Sources and sites of attentional control

Regions of the frontal lobe, including the supplementary eye fields (SEF) and frontal eye fields (FEF),
become active when an individual is directing attention to a location – whether a stimulus is present
or not. The visual cortex is more active once the item is present. So, it seems that prefrontal areas
engage in predicting and preparing attention (= source) while posterior areas serve in processing (=
site).

We may use several mechanisms to direct our attention, such as space-based (“it should be to the
left”, 100ms) versus object-based (170ms) or feature-based (colour, 100ms) attention. Depending on
the mechanism, different sites are involved. Object-based attention includes categories such as
faces, wherein the fusiform face area plays a prominent role. But there are specialized regions for
different object types – bodies, houses, etc.

Oscillation, especially in the gamma-band frequency, seems to couple the sites and sources with
prefrontal regions preceding the signal in posterior regions by about 20 milliseconds, serving as the
“leader”.

Neural mechanisms of selection: biased competition

Suppression of distracting information is another important mechanism of attentional control. It is

mostly connected to alpha-band oscillations of the contralateral hemisphere and less cortical
excitability. The biased-competition model states that ongoing neural activity is analysed to predict or
bias attention and move it to a location relevant for the task. This could be top-down or bottom-up
influences, so either goal-oriented or salience-driven. Additionally, there are feedback processes that
enhance perception based on ongoing processing, reinforcing involved pathways.

4. Neural bases of divided attention

There is no final conclusion about attentional multi-tasking, but some researchers argue that
processing by lateral prefrontal cortex acts as a central bottleneck in resources, which in some cases
makes it impossible to perform two tasks simultaneously. This idea of a central bottleneck is
connected to the model of working memory, relying on executive control.

Other researchers have argued that the overall demands on the brain are greater under divided
compared to single-task conditions. So, two tasks that require use of the same brain regions are
more difficult to perform simultaneously. Evidence shows that this ability to distribute attention in
the same modality varies between individuals.

5. Network models of attentional control

a) A distributed but overlapping network: specialization is not absolute, lesions to different areas of
the attention network can have similar effects. It includes three representations: a sensory
representation in posterior parietal cortex, a schema for distributing exploratory movements in
frontal cortex, and a motivational map in the cingulate cortex.
b) Alerting, orienting and executive attention (Posner): these three serve as separable systems to
attention. The alerting system relies on the locus coeruleus, thalamic regions, and a right-hemisphere
system involved in overall arousal, and is linked to the neurotransmitter norepinephrine. Orienting
relies on the superior colliculus, parietal areas, and the frontal eye fields, and is linked to the
neurotransmitter acetylcholine. Executive attention is composed of the basal ganglia, lateral ventral
prefrontal regions and the anterior cingulate and is thought to rely on dopamine.

c) Selection of goals versus detection of behaviourally relevant stimuli: the dorsal attention system is
involved in top-down processes, while the ventral attention system is responsible for bottom-up
detection. In this manner, the ventral system can interrupt ongoing goal directed tasks (and vice
versa).

d) The Default Network: lack of attention or internal attention? Activity in the default network seems
to have a reciprocal relationship with activity in attentional control structures. Thus, the ability to pay
attention seems to rely not only on engagement of attentional systems, but also on disengagement
of the default mode network. Other perspectives argue that the default network is engaged when we
turn our attention inward, e.g. in self-reflecting, future planning or reasoning about moral. It can be
divided into three subsystems: 1. thinking about information in reference to themselves, 2. mental
simulation, 3. the metacognitive process of inferring or reflecting upon the mental states of other
people and/or one’s self.

Hemineglect

6. Clinical features

Hemineglect is a syndrome in which individuals ignore, or do not pay attention to, the side of space
contralateral to their lesion (most often, the left side is neglected). This may include noticing items
on the left side of the world (i.e., spatial neglect), drawing the left side of objects (i.e., allocentric
neglect), using the left side of the body or even perceiving that it belongs to them. Hemi-extinction
refers to the phenomenon, where stimuli are neglected due to competition from the other
(nonimpaired) side.

Damage to diverse regions can cause neglect, so it is unlikely to arise from damage to just one region,
but rather results from damage to a network of interconnected regions in the right hemisphere.

Hemineglect is caused by disruptions of connectivity and not loss of sensitivity. Very salient or
emotional stimuli can move the attention to the neglected side, as do information critical to
comprehension of material in a context or simply motivational factors such as rewards. However,
patients are not aware that they neglect one side.

Theories

One suggestion is that patients lack an internal mental representation of the neglected side of space.
A study showed that the neglect also shows in reproduction of memory. It could be that the space
toward the periphery is more and more compacted. There is large evidence, though, that
competition between the hemispheres is so strong, that patients just fail to disengage attention from
the nonneglected field. After a salient stimulus in the nonneglected field, it takes much longer for
people with hemineglect to detect a stimulus in the neglected field. Even more, TMS is able to induce
or disrupt the effects of hemineglect: When TMS is applied over the parietal region to deactivate it,
extinction is observed for information in the contralateral space. Conversely, giving TMS to facilitate
brain activity increases attention to the contralateral field.

Treatment

Usually, hemineglect gets better with time, but rarely disappears completely. Magnetic or electric
stimulation works well as long as it’s applied, but effects only last for about two weeks or at least
need ongoing treatment. A number of methods work by inducing the illusory subjective feeling that
there is a drift or movement rightward (e.g. moving the arm passively), which requires a
compensatory leftward orientation to stabilize the world. Optokinetic stimulation works by moving
items that the patient should fixate without moving the head.

Caloric stimulation: Both introducing water that is substantially colder than body temperature to the
left ear, or water that is substantially warmer than body temperature to the right ear, results in the
eyes orienting toward the left. A more modern version of this technique is applying electrical
stimulation to the mastoid bone behind the ear because the vestibular nerve runs just below it. Prism
adaptation: wearing prisms that move the visual world 10 degrees to the right helps in training them
to orient further leftward.

Visual scanning training and virtual reality environment training can be more top-down therapies and
useful in training in a safe environment (e.g., crossing a street).

7. Implications for understanding brain-behaviour relationships

Object-based attention

In object-based neglect, not the spatial location of an object is relevant, but the left half of the
stimulus itself is ignored. Damage that results in object-centered neglect seems to involve lesions
that are a bit more posterior and inferior to those that typically cause neglect. This finding supports
that there are both a space-based and an object-based way of directing attention.

Hemispheric differences in attentional control

Hemineglect is much more prominent and severe after right-hemisphere damage than after left-
hemisphere damage. Not only does each
hemisphere exhibit an attentional bias for
information located in the contralateral space,
but the right hemisphere plays a bigger role in
overall attention and arousal. Right-handed
persons have a bias towards the left side of
space, here a face. Hence, information on the
left is perceived as more salient. So, to right-
handed individuals, the person in picture A appears happier than in B, although they are mirrored.

As mentioned above, TMS can ameliorate attention to the neglected side, but if applied to the left
hemisphere, it also disrupts attention on the ipsilateral side. This does not happen when applied to
the right hemisphere, plus bilateral attention distribution increases activity over the right but not the
left parietal lobe, suggesting that the right hemisphere can distribute attention in a more bilateral
manner than the left.
Processing of unattended stimuli

Some findings provide evidence that information may be processed to some degree even if it doesn’t
reach consciousness. Priming studies have demonstrated that information on the left, which cannot
be explicitly recognized, nonetheless influences performance. There is evidence that priming in the
neglected visual field still works, while it does not for patients that are blind in one visual field.

FMRI studies show that neglected items still evoke activity in similar regions as when they are
consciously perceived, although to a smaller degree. ERPs provide evidence regarding the time point
at which processing of neglected and nonneglected stimuli diverge (ca. 170ms). They are still
processed at early stages, but fail to gain access to higher-order visual processing areas, thus are not
perceived consciously.

These studies reinforce the idea that attention serves to modulate the processing of information:
Attended information is processed more fully, whereas unattended information is processed to a
lesser degree. This modulation occurs at many different points in time and involves many diverse
regions of the cortex.

8. Consciousness

Emerging research suggests that there is not one brain region that is the seat of consciousness, but
rather consciousness is an emergent phenomenon that arises from the interaction of brain
mechanisms and regions. While the study of attention can provide some answers on consciousness,
another idea is to approach more basic and broad mechanisms.

Basically, scientists extract information about two major aspects of brain functioning: one related to
how easily information can be integrated across different regions of the brain, and the other related
to how differentiated patterns of activity are across distinct brain regions. A combination of these
measures is associated with conscious reports of experience across a wide range of conditions,
including variations in consciousness associated with anaesthetics and sleep. These findings suggest
that it is the dynamics of interaction within and between brain regions that helps to define our
different conscious states.