Frontal lobes and executive function
Sam Gilbert
Institute of Cognitive Neuroscience
[email protected]
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
What are executive functions?
• Umbrella term for processes that control and organise behaviour
• Allow us to co-ordinate psychological processes (attention, memory,
language, perception, etc.) in order to achieve goals
• e.g. BLUE
Prefrontal Cortex
Cortical region of the frontal lobe anterior to the primary and association motor
cortices
James (1890): “The anterior frontal lobes, for example, so far as is yet
known, have no de nite functions. […] neither stimulation nor excision of the
prefrontal lobes produces any symptoms whatever.”
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Wilder Pen eld (1891 - 1976)
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Pen eld and Evans (1935)
“Neurological examination on discharge was entirely negative … Two months after operation
she had returned to her own family and during the year which followed lived a happy and
essentially normal life.”
“She looked forward to [making dinner for guests] with pleasure and had the whole day for
preparation. This was a thing she could have done with ease ten years before. When the
appointed hour arrived she was in the kitchen, the food was all there, one or two things were
on the stove, but the salad was not ready, the meat had not been started and she was
distressed and confused by her long continued effort alone. It seemed evident that she would
never be able to get everything ready at once.”
“The defect produced was a lack of capacity for planned administration.”
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Brenda Milner (1918 -)
“The results provide clear evidence of the inability of patients
with dorsolateral frontal-lobe lesions to shift from one sorting
principle to another” (Milner, 1963)
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
What are executive functions?
• Executive functions include:
• Inhibition
• Flexibility
• Planning
• Judgement / synthesis
• Multitasking
What are executive functions?
• Executive functions include:
• Inhibition
RED RED
BLUE BLUE
GREEN GREEN
YELLOW YELLOW
Stroop Task
• Extreme form of inhibitory failure: “utilisation behaviour” (Shallice et al.,
1989)
What are executive functions?
• Executive functions include:
• Flexibility
Wisconsin Card Sorting Test
What are executive functions?
• Executive functions include:
• Planning
Start Aim
Tower of London (Shallice, 1982)
Tower of London (Shallice, 1982)
What are executive functions?
• Executive functions include:
• Judgement / synthesis
How long is the average person’s spine?
How fast does a horse gallop?
How many camels are there in Holland?
How high is the BT Tower?
Cognitive Estimation (Shallice, 1978)
What are executive functions?
• Executive functions include:
• Multitasking
Multiple Errands Test (Shallice & Burgess, 1991)
What are executive functions?
• Executive functions include:
• Multitasking
Healthy Volunteer Patient with Frontal Lobe Injury
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
Supervisory system model (Norman & Shallice, 1986)
• Basic unit of action control: “schema”
• e.g. reading a word, turning on a light switch, answering a phone…
• Schemas can be activated in two qualitatively different ways
Supervisory system model (Norman & Shallice, 1986)
• Contention Scheduling
• primarily bottom-up automatic
triggering in routine situations
• Supervisory Attentional System (SAS),
associated with frontal lobes
• additional top-down control in
non-routine situations
Key point: Supervisory system does not directly control action. It in uences
behaviour by modulating the operation of other systems
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Supervisory system model (Norman & Shallice, 1986)
• Supervisory system required in the following circumstances:
• those that involve planning / decision making
• those that involve error correction / trouble shooting
• situations where responses are not well-learned or contain novel sequences
of actions
• dangerous or technically dif cult situations
• situations that require overcoming of a strong habitual response or resisting
a temptation
In other words: any situation where well-learned behavioural routines will not
suf ce
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Supervisory system model (Norman & Shallice, 1986)
• Model provides account for
performance of patients with
frontal damage on tests of
executive function
• Stroop Task - once activated, dominant scheme “read word” persists in
absence of inhibition by SAS
• Multiple Errands Task - disruption to selection and appropriate sequencing
of schema by SAS leads to disorganised behaviour
Supervisory system model (Norman & Shallice, 1986)
• Can also explain other typical
“frontal” behaviours
• Perseveration - schemes fail to be inhibited after operation
• Distractibility - non-task related schemas capture attention
• Utilisation Behaviour - in absence of supervisory inhibition, attention
captured by information entering perceptual system
Supervisory model ts with what we know of PFC anatomy
“All neural roads eventually lead to the
frontal lobes” (Kolb & Whishaw, 2009)
• Rich interconnections between PFC
subregions
• PFC sends and receives projections
from virtually all major sensory and
motor cortical systems
• Access to highly processed multi-
modal sensory information represented
in higher-order sensory regions
• Subcortical structures (e.g. brainstem,
basal ganglia, cerebellum) project
indirectly to PFC via thalamus
• Perfectly placed to integrate diverse,
high-level representations, and to exert
control over various brain systems
Miller, E.K., & Cohen, J.D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience,
14, 167-202.
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Interim conclusions
• Prefrontal cortex is involved in control / organisation of behaviour
• It does this via modulatory interactions with other brain systems
Outstanding questions
• What are the neurocognitive mechanisms for this?
• Can executive functions be subdivided? If so, how?
• How does this relate to anatomical subdivisions of the prefrontal cortex?
One supervisory system or many?
• Patients with frontal lobe lesions often perform well on some tests but
not on others (e.g. Shallice & Burgess, 1991)
• Behavioural studies suggest factor structure when people perform
multiple executive function tasks
Friedman, N.P. & Miyake, A. (2017). Unity and diversity of executive functions: Individual differences as a
window on cognitive structure. Cortex, 86, 186-204.
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
Homunculus problem
How does the system know when control is required?
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
Lateral frontal cortex: Anterior cingulate:
implements control allocates control
But…
• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
But:
“we nd limited evidence supporting any single dimension that
forms a gradient over lateral frontal cortex, whether that
dimension is one particular type of abstraction or global dif culty”
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• What are executive functions? Why are the frontal lobes thought to be
involved?
• Tasks for measuring executive function
• Supervisory model of executive function
• Models of frontal lobe function and organisation
• a lateral - medial split?
• an anterior - posterior hierarchy?
• a multiple demand system?
How do we nd the right level of description for the
functions of PFC subregions?
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Freedman et al. (2001)
• Monkeys trained to categorise stimuli
as “cats” and “dogs”
• Morphing allowed control over
within-class and between-class
boundaries
• After training, monkeys retrained with
new class boundaries
Freedman, D.J., Riesenhuber, M., Poggio, T., & Miler, E.K. (2001). Categorical representations of visual
stimuli in the primate prefrontal cortex. Science, 291(5502): 312-6.
Freedman et al. (2001)
• Frontal lobe neuronal activity
recorded
• Over 20% neurons differentiated
between “dogs” and “cats”
• After re-training, same neurons now
differentiated between new class
boundaries
Multiple demand model (Duncan, 2010)
• Executive control subserved by a frontoparietal ‘multiple demand
network’
• Neurons in this network exibly code task-speci c information
• Coding can adapt as and when the task or content changes
• Subtle variation in the information coded by different regions, not gross
functional subdivisions
• But: little understanding of how this multiple demand network actually
operates
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Conclusions
• Executive functions: umbrella term for processes that control and organise
behaviour. Measured (indirectly) by various ‘executive function tasks’, which can
be sensitive to frontal lobe damage
• Supervisory model: executive function implemented via modulatory in uence of
a supervisory system
• PFC well-placed to play this role, but mechanisms not fully understood
• There is clearly some degree of functional subdivision, both at a cognitive and
an anatomical level. But details remain controversial.
• Models of PFC organisation:
• Expected value of control - allocation vs implementation of control in medial
vs lateral PFC respectively
• Hierarchical model - posterior to anterior gradient, from low-level motor
control to high-level abstract rules
• Multiple demand system - exible adaptive system with “mosaic”
specialisation rather than gross functional subdivisions
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Readings
General overviews:
Gilbert, S.J., & Burgess, P.W. (2008). Executive Function. Current Biology, 18, R110-114.
Badre, D. (2020). On Task. Princeton University Press.
Expected value of control:
Shenhav, A., Cohen, J.D., & Botvinick, M.M. (2016). Dorsal anterior cingulate and the value of control. Nature Neuroscience, 19,
1286-1291.
Hierarchical model:
Badre, D. & Nee, D.E. (2018). Frontal cortex and the hierarchical control of behaviour. Trends in Cognitive Sciences, 22,
170-188.
Multiple demand model:
Duncan, J. (2010). The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends in
Cognitive Sciences, 14, 172-179.
Duncan, J., Assem, M., & Shashidhara, S. (2020). Integrated intelligence from distributed brain activity. Trends in Cognitive
Sciences, 24, 838-852.
