Relationship between voluntary and involuntary pathways and mechanisms in the frontal lobes

The brain can be divided up into general parts that are thought to be involved in particular roles. One section of the cortex, which contains the parietal, temporal, and occipital lobes is mainly concerned with perception and sensation. The other section is the frontal lobes, and they are mostly concerned with action. The frontal lobes are involved in many aspects of our brain function such as initiation judgement, impulse control, motor function and problem solving. The frontal lobes are the most vulnerable part of the brain due to their position in the cranium, and they exhibit the most wide-ranging deficits after an injury (Levin et al 1987).

Decision-making is thought to be a task that the frontal lobes mediate and evidence for this comes form looking at deficits caused by frontal lobe injuries. Manes et al (2002) suggest that patients that suffer frontal cortex damage display severe impairments in real-life decision-making. This is despite having intact intellect, something that other researchers have also found to occur (Bechara et al 2000, Shallice and Burgess 1991). The Iowa gambling task was devised by Bechara et al (1994), and was intended to test subjects on real-life decision-making. The test consists of four decks of cards that are divided into A and B, which offer high rewards but also high penalties, and decks C and D that offer small rewards but also small penalties. The game is designed so that if the participant chooses more cards from decks C and D, the low reward low penalty deck, they will be money up at the end of the game. The participants were asked to select 100 cards in total, but were unaware that the decks were weighted. If they select cards from decks A and B they receive $100 and if they select cards from C and D they receive $50, but at random they will receive penalties. If they select from A and B the penalty is $125 and if they select from C and D the penalty is $50, resulting in an overall loss for those subjects who consistently choose cards from decks A and B. Bechara et al (1994) suggest that the Iowa gambling game is effective in recreating real-life decision making, as it imitates aspects of real-life such as reward and punishment as well as uncertainty.

By testing participants with frontal lobe damage using the Iowa gambling game, information on the type and specific area of deficits in the frontal lobes can be ascertained. This also helps us to understand in more detail the specific functions and mechanisms of the frontal lobe. Bechara, Tranel and Damasio (2000) demonstrated that patients with bilateral lesions of the ventromedial prefrontal cortex are unaware of future consequences of their decision-making. On the gambling game they failed to detect that the immediate gains of the high reward decks resulted in overall losses, they seemed unable to see past the instant gratification of the high reward deck. Control participants would initially make errors in choice until they realized that the low reward low risk decks eventually resulted in success and the high reward high-risk decks did not. Bechara, Tranel and Damasio (2000) also measured skin conductance response, and found that the patients suffering from lesions of the ventromedial prefrontal cortex had similar reading to that o the control participants. Bechara, Tranel and Damasio (2000) concluded that patients with ventromedial prefrontal lesions are insensitive to future consequences, whether they are positive or negative. They also highlight inhibition, as being a factor in the ventromedial patients responses, implying that the underlying mechanism that governs suppressing voluntary responses is a somatic state. Bechara, Tranel and Damasio (2000) suggest that an emotional signal that biases the choice of a profitable response from a range of options is a factor, but is not the primary cause of the impairment.

Another study conducted by Bechara, Damasio and Damasio (2000) develops the notion of somatic states being involved in decision-making. They explain that a deficit in emotion and feeling that occurs in the orbitofrontal cortex effects decision-making. Somatic states are concerned with conscious and unconscious operations, support processes and knowledge of a situation. Previously activated factual and emotional sets are activated together and an association is made; if consciously activated the process warns the decision maker of the good or bad options available. If the association is unconsciously activated a bias is formed towards a particular option, this allows the decision maker to effectively assess their options and make the best decision quickly. The gambling game was used to assess the performance of patients suffering ventromedial cortex lesions, and found that they exhibited impairments in somatic or emotional processing as well as decision-making. Bechara, Damasio and Damasio (2000) suggest that response inhibition may be one explanation as to why ventromedial patients suffer problems with decision-making. They propose that an error in activating somatic states that give signals as to whether to inhibit a response or not, may account for the poor performance of ventromedial patients on decision-making tasks.

Manes et al (2002) also studied the relationship between frontal lobe damage and deficits in decision-making. As well as the Iowa gambling game two other decision-making tasks and a battery of tests was dispensed assessing memory, planning ability and attentional shifting. Manes at al (2002) looked specifically at patients with discrete orbitofrontal lesions, dorsolateral lesions, dorsomedial lesions and large frontal lesions. They found that the patients with large frontal lesions were the only patients to show impairment on all three decision-making tasks, however the dorsolateral and dorsomedial lesion patients performed poorly on the Iowa gambling game. Manes et al (2002) suggest that a specific type of working memory deficit may account for the poor performance of the dorsolateral lesion patients on the Iowa gambling game. This implication can be seen as complying with Bechara, Damasio and Damasio’s (2000) conclusion that somatic states influence decision making, as they say that somatic states involve different support processes of which memory is one. Although the findings appear to conflict the difference in sample size and type, and the different approach to testing may account for the difference in findings.

Another test that investigates the relationship of mechanisms in the frontal lobes is the Anti-saccades task. This was developed by Hallett (1978) and is designed to make the subject respond to a visual target by performing a saccade in the opposite direction. A saccade is a rapid and intermittent jump of eye position, used to fixate an object with foveal vision (Bruce, Green and Georgeson 1996), and can be voluntary and involuntary. Voluntary eye movement is used when we need to saccade from what we are currently viewing to view new stimuli, or when we have to maintain a fixation on the current stimuli and ignore competing stimuli, involuntary eye movement arises when the eye is drawn to novel stimuli. The anti-saccade task looks at voluntary and inhibitory cognitive controls, which are thought to originate in the frontal cortex (Sweeney et al 1997). The anti-saccade task involves the subjects being shown a fixation mark followed by a peripheral mark either to the left or right of the fixation mark. They are then instructed to ignore the peripheral mark and to look in the opposite direction. Research shows that patients suffering from frontal lesions have trouble performing well on the anti-saccade task (Everling et al 1999, Muri et al 1998, Munoz and Everling 2004).

Everling, Dorris et al (1999) carried out a study that highlights the importance of specific activation patterns in different brain regions. They monitored neural activity in monkeys whilst they performed pro and anti-saccade tasks, and established that during anti-saccade tasks an increase in activity in the superior colliculus

occurred. Specifically they saw a decrease in stimulus and saccade-related activity prior to anti-saccade tasks, which they proposed helped to reduce unwanted pro-saccades (saccades towards peripheral mark). Everling, Dorris et al (1999) suggest that the production of a motor signal is sent to the saccade generator, this must then be modified probably by another signal for an anti-saccade movement to be successful. Pre-stimulus activity was a significant factor in the presentation of correct saccades and anti-saccades, and the ability to suppress the reflexive or involuntary action is important when trying to execute a voluntary anti-saccade (Everling, Dorris et al 1999).

Muri et al (1998) looked at cortical activation pattern in the frontal lobes of healthy individuals during saccade and anti-saccade tasks. They found that activity in the dorsolateral prefrontal cortex increased with anti-saccade tasks compared to activity during saccade tasks. This supports other findings that suggest patients with dorsolateral prefrontal lesions suffer impaired performance on anti-saccade tasks, and Muri et al (1998) propose that this is due to an inability by patients to suppress unwanted responses. Although patients with lesions in areas other than the dorsolateral prefrontal cortex also suffer deficits during performance of anti-saccade tasks, Muri et al (1998) say that this specific area may be linked to the inability to suppress unwanted responses. A review of the anti-saccade task and voluntary control of eye movement by Munoz and Everling (2004) indicates that voluntary control over saccade behaviour is required to perform the anti-saccade task successfully. This requires a participant to voluntarily control an involuntary action, by suppressing the motor reaction to the periphery mark presented during the anti-saccade task. It is this action that is thought to be affected by frontal lobe lesions, which explains why patients who suffer frontal lobe lesions perform poorly on anti-saccade tasks.

Research that investigates the function of the frontal lobes is varied and extensive, due to the vast array of tasks the frontal lobe performs. The areas looked at show that mechanisms of voluntary and involuntary action in the frontal lobes are interconnected and important in managing our behaviour. Studies using the Iowa gambling game have shown how crucial voluntary control over decision-making is and how people who suffer from lesions to parts of the frontal lobe have difficulty controlling involuntary action. The same is true of the research that looks at the anti-saccade task. Having voluntary control over occulomotor movement seems to

originate from the frontal lobes, although not exclusively. The studies that explored patients with frontal cortex lesions performance on anti-saccade tasks, highlighted the need for voluntary suppression of involuntary actions in order to perform well. The more research that is carried out using technology such as magnetic resonance imaging and analysis of cerebral blood flow, the better our understanding of frontal lobe pathways and mechanisms.

References

  • Bechara, A, Damasio, A.R, Damasio, H, Anderson, S.W (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition, 50,1-15.
  • Bechara, A, Damasio, H and Damasio, A.R. (2000). Emotion decision making and the orbitofrontal cortex. Cerebral cortex, 10, 295-307
  • Bechara, A, Tranel, D and Damasio, H. (2000). Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain, 123, 2189-2202.
  • Bruce, V, Green, P.R, and Georgeson, M.A. (1996). Visual perception: Physiology, psychology and ecology (pp21-22). 3rd Edition. UK: Psychology press.
  • Everling, S, Dorris, M.C, Klein, R.M, and Munoz, D.P. (1999). Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. The Journal of neuroscience, 19 (7), 2740-2754.
  • Hallett, P. E. (1978). Primary and secondary saccades to goals defined by instructions. Vision Research, 18, 1279-1296.
  • Levin, H.S, Amparo, E.G, Eisenberg, H.M. (1987). Magnetic resonance imaging and computerized tomography in relation to the neurobehavioral sequelae of mild and moderate head injuries. Journal of
  • Neurosurgery, 66, 706-713.
  • Manes, F, Sahakian, B, Clark, L, Rogers, R, Antoun, N, Aitken, M and Robbins, T. (2002) Decision-making processes following damage to the prefrontal cortex. Brain, 125, 624-639.
  • Munoz, D. P. and Everling, S. (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nature Review. Neuroscience, 5, 218-228.
  • Muri, R.M, Heid, O, Nirkko, A.C, Ozdoba, C, Felblinger, J, Schroth, G and Hess, C.W. (1998) Functional organisation of saccades and anti-saccades in the frontal lobe in humans: a study with echo planar functional magnetic resonance imaging. Journal of Neurology, Neurosurgery and Psychiatry, 65, 34-37.
  • Shallice, T, Burgess, P.W. (1991). Deficits in strategy application following frontal lobe damage in man. Brain, 114, 727-741.
  • Sweeney, J.A, Luna, B, Strojwas, M.H, Thulborn, K.R. (1997). Mapping distinct cortical eye fields for saccadic and pursuit eye movements in humans using fMRI. Society for Neuroscience Abstr, 864, 8.

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