Executive functions is a term synonymous with cognitive control, and used by psychologists and neuroscientists to describe a loosely defined collection of brain processes whose role is to guide thought and behaviour in accordance with internally generated goals or plans. Often, the executive functions are invoked when it is necessary to override responses that may otherwise be automatically elicited by stimuli in the external environment. For example, on being presented with a potentially rewarding stimulus, such as a tasty piece of chocolate cake, the automatic response might be to take a bite. However, where this behaviour conflicts with internal plans (such as having decided not to eat chocolate cake whilst on a diet), the executive functions might be engaged to inhibit this response. The neural mechanisms by which the executive functions are implemented is a topic of ongoing debate in the field of cognitive neuroscience.
- 1 Historical perspective
- 2 Miller & Cohen's (2001) model
- 3 Experimental evidence
- 4 Context-sensitivity of PFC neurons
- 5 Evidence for attentional biasing in sensory regions
- 6 Connectivity between the PFC and sensory regions when executive functions are used
- 7 Top Down Inhibitory Control
- 8 More recent contributions
- 9 References
Although research into the executive functions and their neural basis has increased markedly over the past 5 years, the theoretical framework in which it is situated is not new. In the 1950s, the British psychologist Donald Broadbent drew a distinction between 'automatic' and 'controlled' processes (a distinction characterized more fully by Shiffrin and Schneider in 1977), and introduced the notion of selective attention, to which executive functions are closely allied. In 1975, the US psychologist Michael Posner stated the term cognitive control in his book chapter entitled 'Attention and cognitive control'. The work of influential researchers such as Michael Posner, Joaquin Fuster, Tim Shallice and their colleagues in the 1980s laid much of the groundwork for recent research into executive functions. For example, Posner proposed that there is separate 'executive' branch of the attentional system, which is responsible for focusing attention on selected aspects of the environment. The British neuropsychologist Tim Shallice similarly suggested that attention is regulated by a 'supervisory system', which can override automatic responses in favour of scheduling behaviour on the basis of plans or intentions. Throughout this period, a consensus emerged that this control system is housed in the most anterior portion of the brain, the prefrontal cortex (PFC)
Miller & Cohen's (2001) model
More recently, in 2001, Earl Miller and Jonathan Cohen published an influential article entitled 'An integrative theory of prefrontal cortex function' in which they argue that cognitive control is the primary function of the PFC, and that control is implemented by increasing the gain of sensory or motor neurons that are engaged by task- or goal-relevant elements of the external environment. In a key paragraph, they argue:
'We assume that the PFC serves a specific function in cognitive control: the active maintenance of patterns of activity that represent goals and the means to achieve them. They provide bias signals throughout much of the rest of the brain, affecting not only visual processes but also other sensory modalities, as well as systems responsible for response execution, memory retrieval, emotional evaluation, etc. The aggregate effect of these bias signals is to guide the flow of neural activity along pathways that establish the proper mappings between inputs, internal states, and outputs needed to perform a given task.'
Miller and Cohen draw explicitly upon an earlier theory of visual attention which conceptualises perception of a visual scene in terms of competition among multiple representations - such as colors, individuals, or objects. Selective visual attention acts to 'bias' this competition in favour of certain selected features or representations. For example, imagine that you are waiting at a busy train station for a friend who is wearing a red coat. You are able to selectively narrow the focus of your attention to search for red objects, in the hope of identifying your friend. Desimone and Duncan argue that the brain achieves this by selectively increasing the gain of neurons responsive to the color red, such that output from these neurons is more likely to reach a downstream processing stage, and consequently to guide behaviour. According to Miller and Cohen, this selective attention mechanism is in fact just a special case of cognitive control - one in which the biasing occurs in the sensory domain. According to Miller and Cohen's model, the PFC can exert control over input (sensory) or output (response) neurons, as well as over assemblies involved in memory, or emotion. Cognitive control is mediated by reciprocal connectivity between the PFC and both sensory, limbic, and motor cortices. Within their approach, thus, the term 'cognitive control' is applied to any situation where a biasing signal is used to promote task-appropriate responding, and control thus becomes a crucial component of a wide range of psychological constructs such as selective attention, error monitoring, decision-making, memory inhibition and response inhibition.
Much of the experimental evidence for the neural structures involved in executive functions comes from laboratory tasks such as the Stroop task or the Wisconsin Card Sorting Task (WCST). In the Stroop task, for example, human subjects are asked to read color names presented in conflicting ink colours (for example, the word 'RED' in green ink). Executive functions are needed to perform this task, as the relatively overlearned and automatic behaviour (word reading) has to be inhibited in favour of a less practiced task - naming the ink color. Recent functional neuroimaging studies have shown that two parts of the PFC, the anterior cingulate cortex (ACC) and the dorsolateral prefrontal cortex (DLPFC), are thought to be particularly important for performing this task. However, functional neuroimaging studies alone cannot prove that a given (activated) brain region is critical for task performance - that requires neuropsychology, e.g.  as well as other loss-of-function studies using Transcranial Magnetic Stimulation, e.g. 
Context-sensitivity of PFC neurons
Other evidence for the involvement of the PFC in executive functions comes from single-cell electrophysiology studies in non-human primates, such as the macaque monkey, which have shown that (in contrast to cells in the posterior brain) many PFC neurons are sensitive to a conjunction of a stimulus and a context. For example, PFC cells might respond to a green cue in a condition where that cue signals that a leftwards saccade should be made, but not to a green cue in another experimental context. This is important, because the optimal deployment of executive functions is invariably context-dependent. To quote an example offered by Miller and Cohen, a US resident might have an overlearned response to look left when crossing the road. However, when the 'context' indicates that he or she is in the UK, this response would have to be suppressed in favour of a different stimulus-response pairing (look right when crossing the road). This behavioural repertoire clearly requires a neural system which is able to integrate the stimulus (the road) with a context (US, UK) to cue a behaviour (look left, look right). Current evidence suggests that neurons in the PFC appear to represent precisely this sort of information. Other evidence from single-cell electrophysiology in monkeys implicates ventrolateral PFC (inferior prefrontal convexity) in the control of motor responses. For example, cells have been identified which increase their firing rate to NoGo signals as well as a signal that says "don't look there!"
Evidence for attentional biasing in sensory regions
Electrophysiology and functional neuroimaging studies involving human subjects have been used to describe the neural mechanisms underlying attentional biasing. Most studies have looked for activation at the 'sites' of biasing, such as in the visual or auditory cortices. Early studies employed event-related potentials to reveal that electrical brain responses recorded over left and right visual cortex are enhanced when the subject is instructed to attend to the appropriate (contralateral) side of space. The advent of bloodflow-based neuroimaging techniques such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) has more recently permitted the demonstration that neural activity in a number of sensory regions, including color-, motion-, and face-responsive regions of visual cortex, is enhanced when subjects are directed to attend to that dimension of a stimulus, suggestive of gain control in sensory neocortex. For example, in a typical study, Liu and coworkers presented subjects with arrays of dots moving to the left or right, presented in either red or green. Preceding each stimulus, an instruction cue indicated whether subjects should respond on the basis of the colour or the direction of the dots. Even though colour and motion were present in all stimulus arrays, fMRI activity in colour-sensitive regions (V4) was enhanced when subjects were instructed to attend to the colour, and activity in motion-sensitive regions was increased when subjects were cued to attend to the direction of motion. Several studies have also reported evidence for the biasing signal prior to stimulus onset, with the observation that regions of the frontal cortex tend to come active prior to the onset of an expected stimulus.
Connectivity between the PFC and sensory regions when executive functions are used
Despite the growing currency of the 'biasing' model of executive functions, direct evidence for functional connectivity between the PFC and sensory regions when executive functions are used, is to date rather sparse. Indeed, the only direct evidence comes from studies in which a portion of frontal cortex is damaged, and a corresponding effect is observed far from the lesion site, in the responses of sensory neurons. However, few studies have explored whether this effect is specific to situations where executive functions are required. Other methods for measuring connectivity between distant brain regions, such as correlation in the fMRI response, have yielded indirect evidence that the frontal cortex and sensory regions communicate during a variety of processes thought to engage executive functions, such as working memory, but more research is required to establish how information flows between the PFC and the rest of the brain when executive functions are used.
Top Down Inhibitory Control
Aside from facilitatory or amplificatory mechanisms of control, many authors have argued for inhibitory mechanisms in the domain of response control, memory, selective attention, and emotion.
More recent contributions
In the 6 years which have elapsed since the publication of Miller & Cohen's article, other important evidence for executive functions processes in the prefrontal cortex have been described. One widely-cited review article emphasises the role of the medial part of the PFC in situations where executive functions are likely to be engaged – for example, where it is important to detect errors, identify situations where stimulus conflict may arise, make decisions under uncertainty, or when a reduced probability of obtaining favourable performance outcomes is detected. This review, like many others, highlights interactions between medial and lateral PFC, whereby posterior medial frontal cortex signals the need for increased executive functions and sends this signal on to areas in dorsolateral prefrontal cortex that actually implement control. Another prominent theory emphasises that interactions along the perpendicular axis of the frontal cortex, arguing that a 'cascade' of interactions between anterior PFC, dorsolateral PFC, and premotor cortex guides behaviour in accordance with past context, present context, and current sensorimotor associations respectively.
- Shiffrin, R. M. & Schneider, W. (1977). Controlled and automatic human information processing: II: Perceptual learning, automatic attending, and a general theory. Psychological Review, 84, 127-190.
- Posner, M.I., & Snyder, C.R.R. (1975). Attention and cognitive control. In R. Solso (ed.), Information Processing and Cognition: The Loyola Symposium. Hillsdale, N.J.: Lawrence Erlbaum Associates.
- Posner, M.I. & Petersen, S.E. (1990) The attention system of the human brain. Annual Review of Neuroscience, 13, 25-42
- Shallice, T. (1988). From neuropsychology to mental structure, Cambridge: CUP.
- Miller, E.K. & Cohen, J.D. (2001). An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167-202
- Desimone R, Duncan J (1995). Neural mechanisms of selective visual attention. Annu Rev Neurosci. 1995;18:193-222.
- Fellows LK and Farah MJ. Is anterior cingulate cortex necessary for cognitive control? Brain. 2005 Apr;128 (Pt 4):788-96. Epub 2005 Feb 10.
- Rushworth MF et al. Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. J Neurophysiol. 2002 May;87(5):2577-92
- Sakagami M et al. A code for behavioral inhibition on the basis of color, but not motion, in ventrolateral prefrontal cortex of macaque monkey. J Neurosci. 2001 Jul 1;21(13):4801-8.
- Hasegawa RP et al. Prefrontal neurons coding suppression of specific saccades. Neuron. 2004 Aug 5;43(3):415-25.
- Hillyard SA, Anllo-Vento L (1998). Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci U S A 95:781-7
- Liu T, Slotnick SD, Serences JT, Yantis S (2003). Cortical mechanisms of feature-based attentional control. Cereb. Cortex 13:1334-43.
- Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (1999). Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22:751-61
- Miller BT, D'Esposito M (2005). Searching for "the top" in top-down control. Neuron 48:535-8
- Barcelo F, Suwazono S, Knight RT (2000). Prefrontal modulation of visual processing in humans. Nat Neurosci. 3:399-403
- Fuster JM, Bauer RH, Jervey JP. 1985. Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Res. 330:299–307.
- Gazzaley A, Rissman J, D'esposito M (2004). Functional connectivity during working memory maintenance. Cogn Affect Behav Neurosci. 4:580-99
- Aron AR & Poldrack RA (2006). Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. Journal of Neuroscience 26 2424-2433
- Anderson MC, Green C (2001) Suppressing unwanted memories by executive control. Nature 410:366-369.
- Tipper SP (2001) Does negative priming reflect inhibitory mechanisms? A review and integration of conflicting views. Q J Exp Psychol A 54:321-343.
- Ochsner KN, Gross JJ (2005) The cognitive control of emotion. Trends Cogn Sci 9:242-249
- Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004). The role of the medial frontal cortex in cognitive control. Science 306:443-7
- MM Botvinick, TS Braver, DM Barch, CS Carter, JD Cohen (2001). Conflict monitoring and cognitive control. Psychological Review 108: 624-52
- Koechlin E, Ody C, Kouneiher F (2003). The architecture of cognitive control in the human prefrontal cortex. Science 302:1181-5