Independent circuits in basal ganglia and cortex for the processing of reward and precision feedback

In order to understand human decision making it is necessary to understand how the brain uses feedback to guide goal-directed behavior. The ventral striatum (VS) appears to be a key structure in this function, responding strongly to explicit reward feedback. However, recent results have also shown striatal activity following correct task performance even in the absence of feedback. This raises the possibility that, in addition to processing external feedback, the dopamine-centered reward circuit might regulate endogenous reinforcement signals, like those triggered by satisfaction in accurate task performance. Here we use functional magnetic resonance imaging (fMRI) to test this idea. Participants completed a simple task that garnered both reward feedback and feedback about the precision of performance. Importantly, the design was such that we could manipulate information about the precision of performance within different levels of reward magnitude. Using parametric modulation and functional connectivity analysis we identified brain regions sensitive to each of these signals. Our results show a double dissociation: frontal and posterior cingulate regions responded to explicit reward but were insensitive to task precision, whereas the dorsal striatum - and putamen in particular - was insensitive to reward but responded strongly to precision feedback in reward-present trials. Both types of feedback activated the VS, and sensitivity in this structure to precision feedback was predicted by personality traits related to approach behavior and reward responsiveness. Our findings shed new light on the role of specific brain regions in integrating different sources of feedback to guide goal-directed behavior

Mapping social reward and punishment processing in the human brain:A voxel-based meta-analysis of neuroimaging findings using the social incentive delay task

Social rewards or punishments motivate human learning and behaviour, and alterations in the brain circuits involved in the processing of these stimuli have been linked with several neuropsychiatric disorders. However, questions still remain about the exact neural substrates implicated in social reward and punishment processing. Here, we conducted four Anisotropic Effect Size Signed Differential Mapping voxel-based meta-analyses of fMRI studies investigating the neural correlates of the anticipation and receipt of social rewards and punishments using the Social Incentive Delay task. We found that the anticipation of both social rewards and social punishment avoidance recruits a wide network of areas including the basal ganglia, the midbrain, the dorsal anterior cingulate cortex, the supplementary motor area, the anterior insula, the occipital gyrus and other frontal, temporal, parietal and cerebellar regions not captured in previous coordinate-based meta-analysis. We identified decreases in the BOLD signal during the anticipation of both social reward and punishment avoidance in regions of the default-mode network that were missed in individual studies likely due to a lack of power. Receipt of social rewards engaged a robust network of brain regions including the ventromedial frontal and orbitofrontal cortices, the anterior cingulate cortex, the amygdala, the hippocampus, the occipital cortex and the brainstem, but not the basal ganglia. Receipt of social punishments increased the BOLD signal in the orbitofrontal cortex, superior and inferior frontal gyri, lateral occipital cortex and the insula. In contrast to the receipt of social rewards, we also observed a decrease in the BOLD signal in the basal ganglia in response to the receipt of social punishments. Our results provide a better understanding of the brain circuitry involved in the processing of social rewards and punishment. Furthermore, they can inform hypotheses regarding brain areas where disruption in activity may be associated with dysfunctional social incentive processing during diseas

A revised computational neuroanatomy for motor control

We discuss a new framework for understanding the structure of motor control. Our approach integrates existing models of motor control with the reality of hierarchical cortical processing and the parallel segregated loops that characterize cortical-subcortical connections. We also incorporate the recent claim that cortex functions via predictive representation and optimal information utilization. Our framework assumes each cortical area engaged in motor control generates a predictive model of a different aspect of motor behavior. In maintaining these predictive models, each area interacts with a different part of the cerebellum and basal ganglia. These subcortical areas are thus engaged in domain appropriate system identification and optimization. This refocuses the question of division of function among different cortical areas. What are the different aspects of motor behavior that are predictively modelled? We suggest that one fundamental division is between modelling of task and body while another is the model of state and action. Thus, we propose that the posterior parietal cortex, somatosensory cortex, premotor cortex, and motor cortex represent task state, body state, task action, and body action, respectively. In the second part of this review, we demonstrate how this division of labor can better account for many recent findings of movement encoding, especially in the premotor and posterior parietal cortices

Inside the brain of an elite athlete: The neural processes that support high achievement in sports

Events like the World Championships in athletics and the Olympic Games raise the public profile of competitive sports. They may also leave us wondering what sets the competitors in these events apart from those of us who simply watch. Here we attempt to link neural and cognitive processes that have been found to be important for elite performance with computational and physiological theories inspired by much simpler laboratory tasks. In this way we hope to inspire neuroscientists to consider how their basic research might help to explain sporting skill at the highest levels of performance

Adaptive Functions of the Corpus Striatum: The Past and Future of the R-Complex

The basal ganglia is emerging from the shadow cast by the most conspicuous clinical expression of its dysfunction: motor disorders.What is revealed is the nexus of a widely distributed system which functions in integrating action with cognition, motivation, and affect. Prominent among non-motor functions are striatal involvement in building up of sequences of behavior into meaningful, goal-directed patterns and repertoires and the selection of appropriate learned or innate sequences in concert with their possible predictive control. Further, striatum seems involved in declarative and strategic memory (involving intentional recollection and the management of retrieved memories, respectively). Findings from reptile experiments indicate striatal control over specific assemblies of innate units of behavior that involve autonomic modulation. Its involvement in the appropriate expression of species-typical action patterns in reptiles and primates provides an interesting vantage point from which to interpret its involvement in the assembly of units of behavior into specific adaptive behavioral patterns. For the current version with updated commentary, see https://notes.utk.edu/bio/greenberg.nsf/9e9a470d5230cdda852563ef0059fa56/89b6c6545b8412c185256a2c0060b638?OpenDocumen

The Brain is a Suitability Probability Processor: A macro model of our neural control system

Our world is characterized by growing diversity and complexity, and the effort to manage our affairs in a good way becomes increasingly difficult. This is true for all spheres of life, including culture, economy, technology, science, politics, environment and daily grind. A corresponding development occurs to our understanding of the brain, which is the crucial organ to keep track of everything. The amount of domain specific findings about this organ grows dramatically, what takes preferably place by highly specialized research. But the holistic understanding of the brain is rather more challenged than supported by this development, resulting in a huge lack of knowledge on the systemic level of the neurosciences. Eckhard Schindler faces this dilemma by introducing a macro model of the brain. This is not only an attempt to improve the perception of our most crucial organ, but also to open a door for a better understanding of our species and for ease our life again.:Part 1 - The Brain as Suitability Probability Processor Introduction Neuro basics Purpose, perception and motor control Excitation, inhibition, pattern transformation and circuits Memory Homeostasis, pain, emotions and rewards The SPP model The emoti(onal-moti)vational system The control levels of the central nervous system The attention assessment controller (AAC) Efficiency through delegation and structuring Universal suitability probability evaluation Needs and library of associative-emotivational patterns Higher needs Needs and suitability probability evaluation Suitability probability evaluation and evolution The two types of consciousness Conscious experiences Individual and social consciousness The 4DI model A four-dimensional intelligence concept (4DI) Dynamics of the need hierarchy Social emotivational dependency chains The need for coherence Artificial needs versus growth needs Dynamics in the 3D tension field 3D tensions in the affluent society The tunnel vision paradox Emotivational amplification adaptation Fading consciousness in affluent contexts About the integrative ingredient of 4DI Toe-holds for other disciplines Part 2 - Excursions to the current state of science Introduction Basal ganglia (BG) and frontal cortex Emotion, motivation and memory Cognitive control and emotions Consciousness Psychology Brain and computer The biggest open questions Index of figures Index of tables Reference

Neural and Behavioral Mechanisms of Interval Timing in the Striatum

To guide behavior and learn from its consequences, the brain must represent time over many scales. Yet, the neural signals used to encode time in the seconds to minute range are not known. The striatum is the major input area of the basal ganglia; it plays important roles in learning, motor function and normal timing behavior in the range of seconds to minutes. We investigated how striatal population activity might encode time. To do so, we recorded the electrical activity from striatal neurons in rats performing the serial fixed interval task, a dynamic version of the fixed Interval schedule of reinforcement. The animals performed in conformity with proportional timing, but did not strictly conform to scalar timing predictions, which might reflect a parallel strategy to optimize the adaptation to changes in temporal contingencies and consequently to improve reward rate over the session. Regarding the neural activity, we found that neurons fired at delays spanning tens of seconds and that this pattern of responding reflected the interaction between time and the animals’ ongoing sensorimotor state. Surprisingly, cells rescaled responses in time when intervals changed, indicating that striatal populations encoded relative time. Moreover, time estimates decoded from activity predicted trial-bytrial timing behavior as animals adjusted to new intervals, and disrupting striatal function with local infusion of muscimol led to a decrease in timing performance. Because of practical limitations in testing for sufficiency a biological system, we ran a simple simulation of the task; we have shown that neural responses similar to those we observe are conceptually sufficient to produce temporally adaptive behavior. Furthermore, we attempted to explain temporal processes on the basis of ongoing behavior by decoding temporal estimates from high-speed videos of the animals performing the task; we could not explain the temporal report solely on basis of ongoing behavior. These results suggest that striatal activity forms a scalable population firing rate code for time, providing timing signals that animals use to guide their actions

Optogenetic dissection of neural circuits underlying emotional valence and motivated behaviors

The neural circuits underlying emotional valence and motivated behaviors are several synapses away from both defined sensory inputs and quantifiable motor outputs. Electrophysiology has provided us with a suitable means for observing neural activity during behavior, but methods for controlling activity for the purpose of studying motivated behaviors have been inadequate: electrical stimulation lacks cellular specificity and pharmacological manipulation lacks temporal resolution. The recent emergence of optogenetic tools provides a new means for establishing causal relationships between neural activity and behavior. Optogenetics, the use of genetically-encodable light-activated proteins, permits the modulation of specific neural circuit elements with millisecond precision. The ability to control individual cell types, and even projections between distal regions, allows us to investigate functional connectivity in a causal manner. The greatest consequence of controlling neural activity with finer precision has been the characterization of individual neural circuits within anatomical brain regions as defined functional units. Within the mesolimbic dopamine system, optogenetics has helped separate subsets of dopamine neurons with distinct functions for reward, aversion and salience processing, elucidated GABA neuronal effects on behavior, and characterized connectivity with forebrain and cortical structures. Within the striatum, optogenetics has confirmed the opposing relationship between direct and indirect pathway medium spiny neurons (MSNs), in addition to characterizing the inhibition of MSNs by cholinergic interneurons. Within the hypothalamus, optogenetics has helped overcome the heterogeneity in neuronal cell-type and revealed distinct circuits mediating aggression and feeding. Within the amygdala, optogenetics has allowed the study of intra-amygdala microcircuitry as well as interconnections with distal regions involved in fear and anxiety. In this review, we will present the body of optogenetic studies that has significantly enhanced our understanding of emotional valence and motivated behaviors.Picower Institute for Learning and Memory (Innovation Fund)Whitehall Foundation (2012-08-45)Wade AwardPicower Neurological Disorder Research FundNational Science Foundation (U.S.). Graduate Research Fellowship ProgramIntegrative Neuronal Systems Center (Grant 6926328)Brain and Cognitive Sciences Special Award (1497200)Marcus Fellowship to Honor Norman B. Leventhal (3891441