scholarly journals Neurons in human pre-supplementary motor area encode key computations for value-based choice

2021 ◽  
Author(s):  
Tomas G Aquino ◽  
Jeffrey Cockburn ◽  
Adam N Mamelak ◽  
Ueli Rutishauser ◽  
John P O'Doherty

Adaptive behavior in real-world environments demands that choices integrate over several variables, including the novelty of the options under consideration, their expected value, and uncertainty in value estimation. We recorded neurons from the human pre-supplementary motor area (preSMA), ventromedial prefrontal cortex (vmPFC) and dorsal anterior cingulate to probe how integration over decision variables occurs during decision-making. In contrast to the other areas, preSMA neurons not only represented separate pre-decision variables for each choice option, but also encoded an integrated utility signal and, subsequently, the decision itself. Conversely, post-decision related encoding of variables for the chosen option was more widely distributed and especially prominent in vmPFC. Our findings position the human preSMA as central to the implementation of value-based decisions.

2009 ◽  
Vol 110 (6) ◽  
pp. 1304-1316 ◽  
Author(s):  
Ariel Tankus ◽  
Yehezkel Yeshurun ◽  
Tamar Flash ◽  
Itzhak Fried

Object The supplementary motor area (SMA) plays an important role in planning, initiation, and execution of motor acts. Patients with SMA lesions are impaired in various kinematic parameters, such as velocity and duration of movement. However, the relationships between neuronal activity and these parameters in the human brain have not been fully characterized. This is a study of single-neuron activity during a continuous volitional motor task, with the goal of clarifying these relationships for SMA neurons and other frontal lobe regions in humans. Methods The participants were 7 patients undergoing evaluation for epilepsy surgery requiring implantation of intracranial depth electrodes. Single-unit recordings were conducted while the patients played a computer game involving movement of a cursor in a simple maze. Results In the SMA proper, most of the recorded units exhibited a monotonic relationship between the unit firing rate and hand motion speed. The vast majority of SMA proper units with this property showed an inverse relation, that is, firing rate decrease with speed increase. In addition, most of the SMA proper units were selective to the direction of hand motion. These relationships were far less frequent in the pre-SMA, anterior cingulate gyrus, and orbitofrontal cortex. Conclusions The findings suggest that the SMA proper takes part in the control of kinematic parameters of endeffector motion, and thus lend support to the idea of connecting neuroprosthetic devices to the human SMA.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Luca F. Kaiser ◽  
Theo O. J. Gruendler ◽  
Oliver Speck ◽  
Lennart Luettgau ◽  
Gerhard Jocham

AbstractIn a dynamic world, it is essential to decide when to leave an exploited resource. Such patch-leaving decisions involve balancing the cost of moving against the gain expected from the alternative patch. This contrasts with value-guided decisions that typically involve maximizing reward by selecting the current best option. Patterns of neuronal activity pertaining to patch-leaving decisions have been reported in dorsal anterior cingulate cortex (dACC), whereas competition via mutual inhibition in ventromedial prefrontal cortex (vmPFC) is thought to underlie value-guided choice. Here, we show that the balance between cortical excitation and inhibition (E/I balance), measured by the ratio of GABA and glutamate concentrations, plays a dissociable role for the two kinds of decisions. Patch-leaving decision behaviour relates to E/I balance in dACC. In contrast, value-guided decision-making relates to E/I balance in vmPFC. These results support mechanistic accounts of value-guided choice and provide evidence for a role of dACC E/I balance in patch-leaving decisions.


2018 ◽  
Vol 29 (10) ◽  
pp. 4277-4290 ◽  
Author(s):  
Patrick S Hogan ◽  
Joseph K Galaro ◽  
Vikram S Chib

Abstract The perceived effort level of an action shapes everyday decisions. Despite the importance of these perceptions for decision-making, the behavioral and neural representations of the subjective cost of effort are not well understood. While a number of studies have implicated anterior cingulate cortex (ACC) in decisions about effort/reward trade-offs, none have experimentally isolated effort valuation from reward and choice difficulty, a function that is commonly ascribed to this region. We used functional magnetic resonance imaging to monitor brain activity while human participants engaged in uncertain choices for prospective physical effort. Our task was designed to examine effort-based decision-making in the absence of reward and separated from choice difficulty—allowing us to investigate the brain’s role in effort valuation, independent of these other factors. Participants exhibited subjectivity in their decision-making, displaying increased sensitivity to changes in subjective effort as objective effort levels increased. Analysis of blood-oxygenation-level dependent activity revealed that the ventromedial prefrontal cortex (vmPFC) encoded the subjective valuation of prospective effort, and ACC activity was best described by choice difficulty. These results provide insight into the processes responsible for decision-making regarding effort, partly dissociating the roles of vmPFC and ACC in prospective valuation of effort and choice difficulty.


2021 ◽  
Author(s):  
Timothy P. Morris ◽  
Aaron Kucyi ◽  
Sheeba Arnold Anteraper ◽  
Maiya Rachel Geddes ◽  
Alfonso Nieto-Castañon ◽  
...  

AbstractInformation about a person’s available energy resources is integrated in daily behavioral choices that weigh motor costs against expected rewards. It has been posited that humans have an innate attraction towards effort minimization and that executive control is required to overcome this prepotent disposition. With sedentary behaviors increasing at the cost of millions of dollars spent in health care and productivity losses due to physical inactivity-related deaths, understanding the predictors of sedentary behaviors will improve future intervention development and precision medicine approaches. In 64 healthy older adults participating in a 6-month aerobic exercise intervention, we use neuroimaging (resting state functional connectivity), baseline measures of executive function and accelerometer measures of time spent sedentary to predict future changes in objectively measured time spent sedentary in daily life. Using cross-validation and bootstrap resampling, our results demonstrate that functional connectivity between 1) the anterior cingulate cortex and the supplementary motor area and 2) the right anterior insula and the left temporoparietal/temporooccipital junction, predict changes in time spent sedentary, whereas baseline cognitive, behavioral and demographic measures do not. Previous research has shown activation in and between the anterior cingulate and supplementary motor area as well as in the right anterior insula during effort avoidance and tasks that integrate motor costs and reward benefits in effort-based decision making. Our results add important knowledge toward understanding mechanistic associations underlying complex sedentary behaviors.


2018 ◽  
Vol 71 (6) ◽  
pp. 1276-1280 ◽  
Author(s):  
Sudeep Bhatia ◽  
Timothy L Mullett

Choice option similarity is a key contextual variable in multiattribute choice. Based on theories of preference accumulation, we predicted that decision times would be longer when the available choice options were similar compared with when they were dissimilar, controlling for the relative desirabilities of the options. We tested for the relationship between similarity and decision time in an experiment involving incentivised binary choices between items of equivalent desirability and found that our predictions were confirmed. Our results show how the effects of contextual factors on key decision variables can be accurately predicted by existing computational theories of decision-making.


1998 ◽  
Vol 79 (2) ◽  
pp. 1070-1080 ◽  
Author(s):  
H. Boecker ◽  
A. Dagher ◽  
A. O. Ceballos-Baumann ◽  
R. E. Passingham ◽  
M. Samuel ◽  
...  

Boecker, H., A. Dagher, A. O. Ceballos-Baumann, R. E. Passingham, M. Samuel, K. J. Friston, J.-B. Poline, C. Dettmers, B. Conrad, and D. J. Brooks. Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. J. Neurophysiol. 79: 1070–1080, 1998. The aim of this study was to investigate the functional anatomy of distributed cortical and subcortical motor areas in the human brain that participate in the central control of overlearned complex sequential unimanual finger movements. On the basis of previous research in nonhuman primates, a principal involvement of basal ganglia (medial premotor loops) was predicted for central control of finger sequences performed automatically. In pertinent areas, a correlation of activation levels with the complexity of a motor sequence was hypothesized. H2 15O positron emission tomography (PET) was used in a group of seven healthy male volunteers [mean age 32.0 ± 10.4 yr] to determine brain regions where levels of regional cerebral blood flow (rCBF) correlated with graded complexity levels of five different key-press sequences. All sequences were overlearned before PET and involved key-presses of fingers II–V of the right hand. Movements of individual fingers were kept constant throughout all five conditions by external pacing at 1-Hz intervals. Positive correlations of rCBF with increasing sequence complexity were identified in the contralateral rostral supplementary motor area (pre-SMA) and the associated pallido-thalamic loop, as well as in right parietal area 7 and ipsilateral primary motor cortex (M1). In contrast, while rCBF in contralateral M1 and and extensive parts of caudal SMA was increased compared with rest during task performance, significant correlated increases of rCBF with sequence complexity were not observed. Inverse correlations of rCBF with increasing sequence complexity were identified in mesial prefrontal-, medial temporal-, and anterior cingulate areas. The findings provide further evidence in humans supporting the notion of a segregation of SMA into functionally distinct subcomponents: although pre-SMA was differentially activated depending on the complexity of a sequence of learned finger movements, such modulation was not detectable in caudal SMA (except the most antero-superior part), implicating a motor executive role. Our observations of complexity-correlated rCBF increases in anterior globus palllidus suggest a specific role for the basal ganglia in the process of sequence facilitation and control. They may act to filter and focus input from motor cortical areas as patterns of action become increasingly complex.


2017 ◽  
Author(s):  
Amitai Shenhav ◽  
Mark A. Straccia ◽  
Jonathan D. Cohen ◽  
Matthew M. Botvinick

AbstractDecision-making is typically studied as a sequential process from the selection of what to attend (e.g., between possible tasks, stimuli, or stimulus attributes) to the selection of which actions to take based on the attended information. However, people often gather information across these levels in parallel. For instance, even as they choose their actions, they may continue to evaluate how much to attend other tasks or dimensions of information within a task. We scanned participants while they made such parallel evaluations, simultaneously weighing how much to attend two dynamic stimulus attributes and which response to give based on the attended information. Regions of prefrontal cortex tracked information about the stimulus attributes in dissociable ways, related to either the predicted reward (ventromedial prefrontal cortex) or the degree to which that attribute was being attended (dorsal anterior cingulate, dACC). Within dACC, adjacent regions tracked uncertainty at different levels of the decision, regarding what to attend versus how to respond. These findings bridge research on perceptual and value-based decision-making, demonstrating that people dynamically integrate information in parallel across different levels of decision making.Naturalistic decisions allow an individual to weigh their options within a particular task (e.g., how best to word the introduction to a paper) while also weighing how much to attend other tasks (e.g., responding to e-mails). These different types of decision-making have a hierarchical but reciprocal relationship: Decisions at higher levels inform the focus of attention at lower levels (e.g., whether to select between citations or email addresses) while, at the same time, information at lower levels (e.g., the salience of an incoming email) informs decisions regarding which task to attend. Critically, recent studies suggest that decisions across these levels may occur in parallel, continuously informed by information that is integrated from the environment and from one’s internal milieu1,2.Research on cognitive control and perceptual decision-making has examined how responses are selected when attentional targets are clearly defined (e.g., based on instruction to attend a stimulus dimension), including cases in which responding requires accumulating information regarding a noisy percept (e.g., evidence favoring a left or right response)3-7. Separate research on value-based decision-making has examined how individuals select which stimulus dimension(s) to attend in order to maximize their expected rewards8-11. However, it remains unclear how the accumulation of evidence to select high-level goals and/or attentional targets interacts with the simultaneous accumulation of evidence to select responses according to those goals (e.g., based on the perceptual properties of the stimuli). Recent work has highlighted the importance of such interactions to understanding task selection12-15, multi-attribute decision-making16-18, foraging behavior19-21, cognitive effort22,23, and self-control24-27.While these interactions remain poorly understood, previous research has identified candidate neural mechanisms associated with multi-attribute value-based decision-making11,28,29 and with selecting a response based on noisy information from an instructed attentional target3–5. These research areas have implicated the ventromedial prefrontal cortex (vmPFC) in tracking the value of potential targets of attention (e.g., stimulus attributes)8,11 and the dorsal anterior cingulate cortex (dACC) in tracking an individual’s uncertainty regarding which response to select30–32. It has been further proposed that dACC may differentiate between uncertainty at each of these parallel levels of decision-making (e.g., at the level of task goals or strategies vs. specific motor actions), and that these may be separately encoded at different locations along the dACC’s rostrocaudal axis32,33. However, neural activity within and across these prefrontal regions has not yet been examined in a setting in which information is weighed at both levels within and across trials.Here we use a value-based perceptual decision-making task to examine how people integrate different dynamic sources of information to decide (a) which perceptual attribute to attend and (b) how to respond based on the evidence for that attribute. Participants performed a task in which they regularly faced a conflict between attending the stimulus attribute that offered the greater reward or the attribute that was more perceptually salient (akin to persevering in writing one’s paper when an enticing email awaits). We demonstrate that dACC and vmPFC track evidence for the two attributes in dissociable ways. Across these regions, vmPFC weighs attribute evidence by the reward it predicts and dACC weighs it by its attentional priority (i.e., the degree to which that attribute drives choice). Within dACC, adjacent regions differentiated between uncertainty at the two levels of the decision, regarding what to attend (rostral dACC) versus how to respond (caudal dACC).


2004 ◽  
Vol 91 (6) ◽  
pp. 2734-2746 ◽  
Author(s):  
S. Ohara ◽  
N. E. Crone ◽  
N. Weiss ◽  
R.-D. Treede ◽  
F. A. Lenz

Negative and positive laser evoked potential (LEP) peaks (N2*, P2**) were simultaneously recorded from the primary somatosensory (SI), parasylvian, and medial frontal (MF: anterior cingulate and supplementary motor area) cortical surfaces through subdural electrodes implanted for the surgical treatment of intractable epilepsy. Distribution of the LEP N2* and P2** peaks was estimated to be in cortical areas (SI, parasylvian, and MF) identified by anatomic criteria, by their response to innocuous vibratory stimulation of a finger (v-SEP), and to electrical stimulation of the median nerve (e-SEP). The maximum of the LEP N2* peak was located on the CS, medial (dorsal) to the finger motor area, as determined by cortical stimulation, and to the finger somatosensory area, as determined from the e-SEP and v-SEP. This finding suggests that the generator source of the LEP N2* peak in SI was different from that of e-SEP or v-SEP in Brodmann's areas 3b or 1. In parasylvian and MF, polarity reversal was often observed, indicating tangential current sources in these regions. In contrast to e-SEP and v-SEP, the LEP N2* latency over SI was not shorter than that over the parasylvian region. The amplitude of N2* was larger over SI than over MF and the latencies of the LEP peaks in those 2 regions were different. These findings provide evidence for a significant LEP generator in the postcentral gyrus, perhaps SI cortex, that is situated outside the tactile homunculus in SI and that receives its input arising from nociceptors simultaneously with parasylvian and MF cortex.


2009 ◽  
Vol 27 (2) ◽  
pp. E9 ◽  
Author(s):  
Marec von Lehe ◽  
Johannes Schramm

Object In this paper, the authors' goal was to summarize their experience with the surgical treatment of gliomas arising from the cingulate gyrus. Methods The authors analyzed preoperative data, surgical strategies, complications, and functional outcome in a series of 34 patients (mean age 42 years, range 12–69 years; 14 females) who underwent 38 operations between May 2001 and November 2008. Results In 7 cases (18%) the tumor was located in the posterior (parietal) part of the cingulate gyrus, and in 31 (82%) the tumor was in the anterior (frontal) part. In 10 cases (26%) the glioma was solely located in the cingulate gyrus, and in 28 cases (74%) the tumor extended to the supracingular frontal/parietal cortex. Most cases (23 [61%]) had seizures as the presenting symptom, 8 patients (24%) suffered from a hemiparesis/hemihypesthesia, and 4 patients (12%) had aphasic symptoms. The authors chose an interhemispheric approach for tumor resection in 11 (29%) and a transcortical approach in 27 (71%) cases; intraoperative electrophysiological monitoring was applied in 23 (61%) and neuronavigation in 15 (39%) cases. A > 90% resection was achieved in 32 (84%) and > 70% in another 5 (13%) cases. Tumors were classified as low-grade gliomas in 11 cases (29%). A glioblastoma multiforme (WHO Grade IV, 10 cases [26%]) and oligoastrocytoma (WHO Grade III, 9 cases [24%]) were the most frequent histopathological results. Postoperatively, patients in 13 cases suffered from a transient supplementary motor area syndrome (34%), all of whom had tumors in the anterior cingulate gyrus. In the early postoperative period (30 days) a new deficit occurred in 5 cases (13%, mild motor deficits or aphasic symptoms). One patient had a major bleeding episode 2 days after surgery and was in a persistent vegetative state. Conclusions Gliomas arising from the cingulate gyrus are rare. A gross-total resection is often possible and acceptably safe; intraoperative monitoring and neuronavigation are helpful adjuncts. In case of resection of gliomas arising from the anterior cingulate gyrus a supplementary motor area syndrome has to be considered, particularly when the tumor extends to the supracingular cortex


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