fMRI evidence for a dual process account of the speed-accuracy tradeoff in decision-making

Background

The speed and accuracy of decision-making have a well-known trading relationship: hasty decisions are more prone to errors while careful, accurate judgments take more time. Despite the pervasiveness of this speed-accuracy trade-off (SAT) in decision-making, its neural basis is still unknown.

Methodology/Principal Findings

Using functional magnetic resonance imaging (fMRI) we show that emphasizing the speed of a perceptual decision at the expense of its accuracy lowers the amount of evidence-related activity in lateral prefrontal cortex. Moreover, this speed-accuracy difference in lateral prefrontal cortex activity correlates with the speed-accuracy difference in the decision criterion metric of signal detection theory. We also show that the same instructions increase baseline activity in a dorso-medial cortical area involved in the internal generation of actions.

Conclusions/Significance

These findings suggest that the SAT is neurally implemented by modulating not only the amount of externally-derived sensory evidence used to make a decision, but also the internal urge to make a response. We propose that these processes combine to control the temporal dynamics of the speed-accuracy trade-off in decision-making.     

Temporal and Motor Representation of Rhythm in Fronto-Parietal Cortical Areas: An fMRI Study

When sounds occur with temporally structured patterns, we can feel a rhythm. To memorize a rhythm, perception of its temporal patterns and organization of them into a hierarchically structured sequence are necessary. On the other hand, rhythm perception can often cause unintentional body movements. Thus, we hypothesized that rhythm information can be manifested in two different ways; temporal and motor representations. The motor representation depends on effectors, such as the finger or foot, whereas the temporal representation is effector-independent. We tested our hypothesis with a working memory paradigm to elucidate neuronal correlates of temporal or motor representation of rhythm and to reveal the neural networks associated with these representations. We measured brain activity by fMRI while participants memorized rhythms and reproduced them by tapping with the right finger, left finger, or foot, or by articulation. The right inferior frontal gyrus and the inferior parietal lobule exhibited significant effector-independent activations during encoding and retrieval of rhythm information, whereas the left inferior parietal lobule and supplementary motor area (SMA) showed effector-dependent activations during retrieval. These results suggest that temporal sequences of rhythm are probably represented in the right fronto-parietal network, whereas motor sequences of rhythm can be represented in the SMA-parietal network.     

Flight motor pattern in flying and non-flying Phasmida

Summary The insect order Phasmida comprises species with a broad spectrum of wing morphism and flight ability. By monitoring the electrical activity of several pterothoracic muscles the motor output during tethered flight was recorded for several Phasmida, ranging from excellent fliers to non-winged species. Both winged and non-winged species can generate a motor pattern as judged by criteria used to identify the locust flight pattern. However, in non-fliers the probability of expressing this pattern, its duration and precision are reduced. The antagonistic activity of the chosen muscle pairs is clearly different from the motor output during leg movements, which argues for specific motoneuronal coordination released for different behavioural performances. The demonstration of flight motor output in all tested Phasmida indicates that neural structures including their functional connectivity can be maintained independently of the appropriate peripheral structures. With respect to evolution this supports the idea that central neuronal interactions can be more conservative compared to changes in the periphery. Abbreviations of species names and indication of sexes are given in the first paragraph of Results     

Contribution of area MT to stereoscopic depth perception: choice-related response modulations reflect task strategy

Due to the diversity of tuning properties in sensory cortex, only a fraction of neurons are engaged in a particular task. Characterizing the tuning properties of neurons that are functionally linked to behavior is essential for understanding how activity is "read out" from sensory maps to guide decisions. We recorded from middle temporal (MT) neurons while monkeys performed a depth discrimination task, and we characterized the linkage between MT responses and behavioral choices. Trial-to-trial response fluctuations of MT neurons with odd-symmetric ("Near," "Far") disparity tuning were predictive of monkeys' choices, whereas responses of neurons with even-symmetric tuning were not. This result cannot be explained by neuronal sensitivity or any other response property of MT neurons that we examined but is simply explained by the task strategy that monkeys learned during training. We suggest that this approach provides a physiological means to explore how task strategies are implemented in the brain.     

Subcutaneous adipose tissue pattern in lean and obese women with polycystic ovary syndrome

The new optical device, Lipometer, permits the noninvasive, quick, safe, and precise measurement of the thickness of subcutaneous adipose tissue (SAT) layers at any given site of the human body. Fifteen anatomically well-defined body sites from neck to calf describe the SAT topography (SAT-Top) like an individual "fingerprint." SAT-Top was examined in 33 women with polycystic ovary syndrome (PCOS), in 87 age-matched healthy controls and in 20 Type-II diabetic women. SAT-Top differences of these three groups were described, and, based on a hierarchical cluster analysis, two distinctly different groups of PCOS women, a lean (PCOS(L)) and an obese (PCOS(O)) cluster, were found. For visual comparison of the different types of body fat distribution, the 15-dimensional body fat information was condensed to a two-dimensional factor plot by factor analysis. For comparison of the PCOS like body fat distribution with the "healthy" fat pattern, the (previously published) SAT-Top results of 590 healthy women and men (20-70 years old) and 162 healthy girls and boys (7-11 years old) were added to the factor plot. PCOS(O) women showed a SAT-Top pattern very similar to that of women with Type-II diabetes, even though the diabetic women were on average 30 years older. Compared with their healthy controls, SAT-Top of these PCOS(O) patients was strongly skewed into the android direction, providing significantly decreased leg SAT development and significantly higher upper body obesity. Compared with healthy women, PCOS(L) patients had significantly lower total SAT development (even though height, weight, and body mass index did not deviate significantly), showing a slightly lowered amount of body fat in the upper region and a highly significant leg SAT reduction. This type of fat pattern is the same as found in girls and boys before developing their sex specific body fat distribution. We conclude that women with PCOS develop an android SAT-Top, but compared in more detail, we found two typical types of body fat distribution: the "childlike" SAT pattern in lean PCOS patients, and the "diabetic" body fat distribution in obese PCOS women.     

Mere expectation to move causes attenuation of sensory signals

When a part of the body moves, the sensation evoked by a probe stimulus to that body part is attenuated. Two mechanisms have been proposed to explain this robust and general effect. First, feedforward motor signals may modulate activity evoked by incoming sensory signals. Second, reafferent sensation from body movements may mask the stimulus. Here we delivered probe stimuli to the right index finger just before a cue which instructed subjects to make left or right index finger movements. When left and right cues were equiprobable, we found attenuation for stimuli to the right index finger just before this finger was cued (and subsequently moved). However, there was no attenuation in the right finger just before the left finger was cued. This result suggests that the movement made in response to the cue caused 'postdictive' attenuation of a sensation occurring prior to the cue. In a second experiment, the right cue was more frequent than the left. We now found attenuation in the right index finger even when the left finger was cued and moved. This attenuation linked to a movement that was likely but did not in fact occur, suggests a new expectation-based mechanism, distinct from both feedforward motor signals and postdiction. Our results suggest a new mechanism in motor-sensory interactions in which the motor system tunes the sensory inputs based on expectations about future possible actions that may not, in fact, be implemented.     

Risk Preferences and Prenatal Exposure to Sex Hormones for Ladinos

Risk preferences drive much of human decision making including investment, career and health choices and many more. Thus, understanding the determinants of risk preferences refines our understanding of choice in a broad array of environments. We assess the relationship between risk preferences, prenatal exposure to sex hormones and gender for a sample of Ladinos, which is an ethnic group comprising 62.86% of the population of Guatemala. Prenatal exposure to sex hormones has organizational effects on brain development, and has been shown to partially explain risk preferences for Caucasians. We measure prenatal exposure to sex hormones using the ratio of the length of the index finger to the length of the ring finger (2D:4D), which is negatively (positively) correlated with prenatal exposure to testosterone (estrogen). We find that Ladino males are less risk averse than Ladino females, and that Ladino males have lower 2D:4D ratios than Ladino females on both hands. We find that the 2D:4D ratio does not explain risk preferences for Ladinos. This is true for both genders, and both hands. Our results highlight the importance of exploring the behavioral significance of 2D:4D in non-Caucasian racial groups.     

Android subcutaneous adipose tissue topography in lean and obese women suffering from PCOS: comparison with type 2 diabetic women

The new optical device, the lipometer, enables the noninvasive, quick, safe, and precise determination of the thickness of subcutaneous adipose tissue (SAT) layers at any given site of the human body. Fifteen anatomically well-defined body sites from neck to calf describe a SAT topography (SAT-Top) like an individual "fingerprint" of a subject. This SAT-Top was examined in 16 women with polycystic ovary syndrome (PCOS) and compared to the body fat distribution of 87 age-matched healthy controls and 20 type-2 diabetic women. SAT-Top differences of these three groups were described and, to render the possibility of visual comparison, the 15-dimensional body fat information was condensed to a two-dimensional factor plot by factor analysis. All PCOS patients had an android body fat distribution with significantly thinner SAT layers on the legs as compared to healthy controls. Moreover, a hierarchical cluster analysis resulted in two distinctly different groups of PCOS women, a lean (PCOSL) and an obese (PCOSO) cluster: compared to healthy women, lean PCOS patients had significantly lower total SAT development, even though height, weight, and body mass index did not deviate significantly. Especially on the legs, their SAT layers were significantly lowered, indicating a more "apple-like" fat distribution type. Obese PCOS women showed a SAT-Top pattern very similar to that of women with type-2 diabetes, although the mean age difference between these groups was more than 30 years. Compared to healthy controls, the SAT-Top of these obese PCOS patients was strongly shifted into the android direction, appearing as "super-apples" with a significantly increased upper trunk obesity to 237.8% and a significantly decreased leg SAT development to 79.8%.     

Grid cells, place cells, and geodesic generalization for spatial reinforcement learning

Reinforcement learning (RL) provides an influential characterization of the brain's mechanisms for learning to make advantageous choices. An important problem, though, is how complex tasks can be represented in a way that enables efficient learning. We consider this problem through the lens of spatial navigation, examining how two of the brain's location representations--hippocampal place cells and entorhinal grid cells--are adapted to serve as basis functions for approximating value over space for RL. Although much previous work has focused on these systems' roles in combining upstream sensory cues to track location, revisiting these representations with a focus on how they support this downstream decision function offers complementary insights into their characteristics. Rather than localization, the key problem in learning is generalization between past and present situations, which may not match perfectly. Accordingly, although neural populations collectively offer a precise representation of position, our simulations of navigational tasks verify the suggestion that RL gains efficiency from the more diffuse tuning of individual neurons, which allows learning about rewards to generalize over longer distances given fewer training experiences. However, work on generalization in RL suggests the underlying representation should respect the environment's layout. In particular, although it is often assumed that neurons track location in Euclidean coordinates (that a place cell's activity declines "as the crow flies" away from its peak), the relevant metric for value is geodesic: the distance along a path, around any obstacles. We formalize this intuition and present simulations showing how Euclidean, but not geodesic, representations can interfere with RL by generalizing inappropriately across barriers. Our proposal that place and grid responses should be modulated by geodesic distances suggests novel predictions about how obstacles should affect spatial firing fields, which provides a new viewpoint on data concerning both spatial codes.     

Als ‘A’ niet meer als ‘a’ wordt herkend. Een analyse van verworven woordblindheid

A right-handed patient, aged 72, manifested alexia without agraphia, a right homonymous hemianopia and an impaired ability to identify visually presented objects. He was completely unable to read words aloud and severely deficient in naming visually presented letters. He responded to orthographic familiarity in the lexical decision tasks of the Psycholinguistic Assessments of Language Processing in Aphasia (PALPA) rather than to the lexicality of the letter strings. He was impaired at deciding whether two letters of different case (e.g., A, a) are the same, though he could detect real letters from made-up ones or from their mirror image. Consequently, his core deficit in reading was posited at the level of the abstract letter identifiers. When asked to trace a letter with his right index finger, kinesthetic facilitation enabled him to read letters and words aloud. Though he could use intact motor representations of letters in order to facilitate recognition and reading, the slow, sequential and error-prone process of reading letter by letter made him abandon further training.     

Discounting the freedom to choose: implications for the paradox of choice

Organisms prefer to make their own choices. However, emerging research from behavioral decision making sciences has demonstrated that there are boundaries to the preference for choice. Specifically, many decision makers find an extensive array of choice options to be aversive, often leading to negative emotional states and poor behavioral outcomes. This study examined the degree to which human participants discounted hypothetical rewards that were (a) delayed, (b) probabilistic, and (c) chosen from a large array of options. The present results suggest that the "paradox of choice" effect may be explained within a discounting model for individual patterns of decision making.     

Motor learning with unstable neural representations

It is often assumed that learning takes place by changing an otherwise stable neural representation. To test this assumption, we studied changes in the directional tuning of primate motor cortical neurons during reaching movements performed in familiar and novel environments. During the familiar task, tuning curves exhibited slow random drift. During learning of the novel task, random drift was accompanied by systematic shifts of tuning curves. Our analysis suggests that motor learning is based on a surprisingly unstable neural representation. To explain these results, we propose that motor cortex is a redundant neural network, i.e., any single behavior can be realized by multiple configurations of synaptic strengths. We further hypothesize that synaptic modifications underlying learning contain a random component, which causes wandering among synaptic configurations with equivalent behaviors but different neural representations. We use a simple model to explore the implications of these assumptions.     

Concurrent word generation and motor performance: further evidence for language-motor interaction

Embodied/modality-specific theories of semantic memory propose that sensorimotor representations play an important role in perception and action. A large body of evidence supports the notion that concepts involving human motor action (i.e., semantic-motor representations) are processed in both language and motor regions of the brain. However, most studies have focused on perceptual tasks, leaving unanswered questions about language-motor interaction during production tasks. Thus, we investigated the effects of shared semantic-motor representations on concurrent language and motor production tasks in healthy young adults, manipulating the semantic task (motor-related vs. nonmotor-related words) and the motor task (i.e., standing still and finger-tapping). In Experiment 1 (n = 20), we demonstrated that motor-related word generation was sufficient to affect postural control. In Experiment 2 (n = 40), we demonstrated that motor-related word generation was sufficient to facilitate word generation and finger tapping. We conclude that engaging semantic-motor representations can have a reciprocal influence on motor and language production. Our study provides additional support for functional language-motor interaction, as well as embodied/modality-specific theories.     

Fractional Anisotropy in Corpus Callosum Is Associated with Facilitation of Motor Representation during Ipsilateral Hand Movements

Background

Coactivation of primary motor cortex ipsilateral to a unilateral movement (M1_ipsilateral) has been observed, and the magnitude of activation is influenced by the contracting muscles. It has been suggested that the microstructural integrity of the callosal motor fibers (CMFs) connecting M1 regions may reflect the observed response. However, the association between the structural connectivity of CMFs and functional changes in M1_ipsilateral remains unclear. The purpose of this study was to investigate the relationship between functional changes within M1_ipsilateral during unilateral arm or leg movements and the microstructure of the CMFs connecting both homotopic representations (arm or leg).

Methods

Transcranial magnetic stimulation was used to assess changes in motor evoked potentials (MEP) in an arm muscle during unilateral movements compared to rest in fifteen healthy adults. Functional magnetic resonance imaging was then used to identify regions of M1 associated with either arm or leg movements. Diffusion-weighted imaging data was acquired to generate CMFs for arm and leg areas using the areas of activation from the functional imaging as seed masks. Individual values of regional fractional anisotropy (FA) of arm and leg CMFs was then calculated by examining the overlap between CMFs and a standard atlas of corpus callosum.

Results

The change in the MEP was significantly larger in the arm movement compared to the leg movement. Additionally, regression analysis revealed that FA in the arm CMFs was positively correlated with the change in MEP during arm movement, whereas a negative correlation was observed during the leg movement. However, there was no significant relationship between FA in the leg CMF and the change in MEP during the movements.

Conclusions

These findings suggest that individual differences in interhemispheric structural connectivity may be used to explain a homologous muscle-dominant effect within M1_ipsilateral hand representation during unilateral movement with topographical specificity.     

Cortical preparatory activity: representation of movement or first cog in a dynamical machine?

The motor cortices are active during both movement and movement preparation. A common assumption is that preparatory activity constitutes a subthreshold form of movement activity: a neuron active during rightward movements becomes modestly active during preparation of a rightward movement. We asked whether this pattern of activity is, in fact, observed. We found that it was not: at the level of a single neuron, preparatory tuning was weakly correlated with movement-period tuning. Yet, somewhat paradoxically, preparatory tuning could be captured by a preferred direction in an abstract "space" that described the population-level pattern of movement activity. In fact, this relationship accounted for preparatory responses better than did traditional tuning models. These results are expected if preparatory activity provides the initial state of a dynamical system whose evolution produces movement activity. Our results thus suggest that preparatory activity may not represent specific factors, and may instead play a more mechanistic role.     

Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults.

A steadiness-improving intervention was used to determine the contribution of variability in motor unit discharge rate to the fluctuations in index finger acceleration and manual dexterity in older adults. Ten healthy and sedentary old adults (age 72.9 +/- 5.8 yr; 5 men) participated in the study involving abduction of the left index finger. Single motor unit activity was recorded in the first dorsal interosseus muscle before, after 2 wk of light-load training (10% maximal load), and after 4 wk of heavy-load training (70% maximal load). As expected, the light-load training was effective in reducing the fluctuations in index finger acceleration during slow shortening (0.25 +/- 0.12 to 0.13 +/- 0.08 m/s(2)) and lengthening contractions (0.29 +/- 0.10 to 0.14 +/- 0.06 m/s(2)). Along with the decline in the magnitude of the fluctuations, there was a parallel decrease in the coefficient of variation for discharge rate during both contraction types (33.8 +/- 6.8 to 25.0 +/- 5.9%). The heavy-load training did not further improve either the fluctuations in acceleration or discharge rate variability. Furthermore, the manual dexterity of the left hand improved significantly with training (Purdue pegboard test: 11 +/- 3 to 14 +/- 1 pegs). Bivariate correlations indicated that the reduction in fluctuations in motor output during shortening (r(2) = 0.24) and lengthening (r(2) = 0.14) contractions and improvement in manual dexterity (r(2) = 0.26) was directly associated with a decline in motor unit discharge rate variability. There was a strong association between the fluctuations in motor output and manual dexterity (r(2) = 0.56). These results indicate that practice of a simple finger task was accompanied by a reduction in the discharge rate variability of motor units, a decrease in the fluctuations in motor output of a hand muscle, and an improvement in the manual dexterity of older adults.     

Participation of primary motor cortex in the programming of muscle activity during catching of a falling object

A sitting person has been exposed to transcranial magnetic stimulation (TMS) of the primary motor cortex shortly before and during increasing anticipatory grip force, while an object was falling into a cup held between the thumb and index finger of the subject. Comparison of the changes in the electrical activity of adductor pollicis brevis and the first dorsal interosseous muscles and of TMS response in these muscles revealed, on the one hand, a strong increase in TMS response not long before enhancement of muscle activity and, on the other hand, an insignificant increase in the response amplitude during substantial increase in muscle activity. An increase in the TMS response prior to initiation of motor activity suggests that the excitability of the primary motor cortex is enhanced due to specific processes caused by the direct involvement of the cortex in the programming of motor activity.     

Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex

The prefrontal cortex (PFC) receives substantial anatomical input from the amygdala, and these two structures have long been implicated in reward-related learning and decision making. Yet little is known about how these regions interact, especially in humans. We investigated the contribution of the amygdala to reward-related signals in PFC by scanning two rare subjects with focal bilateral amygdala lesions using fMRI. The subjects performed a reversal learning task in which they first had to learn which of two choices was the more rewarding, and then flexibly switch their choices when contingencies changed. Compared with healthy controls, both amygdala lesion subjects showed a profound change in ventromedial prefrontal cortex (vmPFC) activity associated with reward expectation and behavioral choice. These findings support a critical role for the human amygdala in establishing expected reward representations in PFC, which in turn may be used to guide behavioral choice.     

Corticospinal Excitability Modulation During Action Observation

This study used the transcranial magnetic stimulation/motor evoked potential (TMS/MEP) technique to pinpoint when the automatic tendency to mirror someone else''s action becomes anticipatory simulation of a complementary act. TMS was delivered to the left primary motor cortex corresponding to the hand to induce the highest level of MEP activity from the abductor digiti minimi (ADM; the muscle serving little finger abduction) as well as the first dorsal interosseus (FDI; the muscle serving index finger flexion/extension) muscles. A neuronavigation system was used to maintain the position of the TMS coil, and electromyographic (EMG) activity was recorded from the right ADM and FDI muscles. Producing original data with regard to motor resonance, the combined TMS/MEP technique has taken research on the perception-action coupling mechanism a step further. Specifically, it has answered the questions of how and when observing another person''s actions produces motor facilitation in an onlooker''s corresponding muscles and in what way corticospinal excitability is modulated in social contexts.     

Parallel motor pathways from thoracic interneurons of the ventral giant interneuron system of the cockroach, Periplaneta americana

The data described here complete the principal components of the cockroach wind-mediated escape circuit from cercal afferents to leg motor neurons. It was previously known that the cercal afferents excite ventral giant interneurons which then conduct information on wind stimuli to thoracic ganglia. The ventral giant interneurons connect to a large population of interneurons in the thoracic ganglia which, in turn, are capable of exciting motor neurons that control leg movements. Thoracic interneurons that receive constant short latency inputs from ventral giant interneurons have been referred to as type A thoracic interneurons (TIAs). In this paper, we demonstrate that the motor response of TIAs occurs in adjacent ganglia as well as in the ganglion of origin for the TIA. We then describe the pathway from TIAs to motor neurons in both ganglia. Our observations reveal complex interactions between thoracic interneurons and leg motor neurons. Two parallel pathways exist. TIAs excite leg motor neurons directly and via local interneurons. Latency and amplitude of post-synaptic potentials (PSPs) in motor neurons and local interneurons either in the ganglion of origin or in adjacent ganglia are all similar. However, the sign of the responses recorded in local interneurons (LI) and motor neurons varies according to the TIA subpopulation based on the location of their cell bodies. One group, the dorsal posterior group, (DPGs) has dorsal cell bodies, whereas the other group, the ventral median cells, (VMC) has ventral cell bodies. All DPG interneurons either excited postsynaptic cells or failed to show any connection at all. In contrast, all VMC interneurons either inhibited postsynaptic cells or failed to show any connection. It appears that the TIAs utilize directional wind information from the ventral giant interneurons to make a decision on the optimal direction of escape. The output connections, which project not only to cells within the ganglion of origin but also to adjacent ganglia and perhaps beyond, could allow this decision to be made throughout the thoracic ganglia as a single unit. However, nothing in these connections indicates a mechanism for making appropriate coordinated leg movements. Because each pair of legs plays a unique role in the turn, this coordination should be controlled by circuits dedicated to each leg. We suggest that this is accomplished by local interneurons between TIAs and leg motor neurons.