Marco K. Wittmann

Multiple signals in anterior cingulate cortex.

Highlights • There are multiple signals in anterior cingulate cortex (ACC).• ACC activity reflects value of behavioural change even after controlling for difficulty.• ACC activity reflects updating of internal models even after controlling for difficulty.

Value, search, persistence and model updating in anterior cingulate cortex

Dorsal anterior cingulate cortex (dACC) carries a wealth of value-related information necessary for regulating behavioral flexibility and persistence. It signals error and reward events informing decisions about switching or staying with current behavior. During decision-making, it encodes the average value of exploring alternative choices (search value), even after controlling for response selection difficulty, and during learning, it encodes the degree to which internal models of the environment and current task must be updated. dACC value signals are derived in part from the history of recent reward integrated simultaneously over multiple time scales, thereby enabling comparison of experience over the recent and extended past. Such ACC signals may instigate attentionally demanding and difficult processes such as behavioral change via interactions with prefrontal cortex. However, the signal in dACC that instigates behavioral change need not itself be a conflict or difficulty signal.

Multiple Neural Mechanisms of Decision Making and Their Competition under Changing Risk Pressure

Summary Sometimes when a choice is made, the outcome is not guaranteed and there is only a probability of its occurrence. Each individual’s attitude to probability, sometimes called risk proneness or aversion, has been assumed to be static. Behavioral ecological studies, however, suggest such attitudes are dynamically modulated by the context an organism finds itself in; in some cases, it may be optimal to pursue actions with a low probability of success but which are associated with potentially large gains. We show that human subjects rapidly adapt their use of probability as a function of current resources, goals, and opportunities for further foraging. We demonstrate that dorsal anterior cingulate cortex (dACC) carries signals indexing the pressure to pursue unlikely choices and signals related to the taking of such choices. We show that dACC exerts this control over behavior when it, rather than ventromedial prefrontal cortex, interacts with posterior cingulate cortex.

Predictive decision making driven by multiple time-linked reward representations in the anterior cingulate cortex

In many natural environments the value of a choice gradually gets better or worse as circumstances change. Discerning such trends makes predicting future choice values possible. We show that humans track such trends by comparing estimates of recent and past reward rates, which they are able to hold simultaneously in the dorsal anterior cingulate cortex (dACC). Comparison of recent and past reward rates with positive and negative decision weights is reflected by opposing dACC signals indexing these quantities. The relative strengths of time-linked reward representations in dACC predict whether subjects persist in their current behaviour or switch to an alternative. Computationally, trend-guided choice can be modelled by using a reinforcement-learning mechanism that computes a longer-term estimate (or expectation) of prediction errors. Using such a model, we find a relative predominance of expected prediction errors in dACC, instantaneous prediction errors in the ventral striatum and choice signals in the ventromedial prefrontal cortex.

Self-Other Mergence in the Frontal Cortex during Cooperation and Competition

Summary To survive, humans must estimate their own ability and the abilities of others. We found that, although people estimated their abilities on the basis of their own performance in a rational manner, their estimates of themselves were partly merged with the performance of others. Reciprocally, their ability estimates for others also reflected their own, as well as the others’, performance. Self-other mergence operated in a context-dependent manner: interacting with high or low performers, respectively, enhanced and diminished own ability estimates in cooperative contexts, but the opposite occurred in competitive contexts. Self-other mergence not only influenced subjective evaluations, it also affected how people subsequently objectively adjusted their performance. Perigenual anterior cingulate cortex tracked one’s own performance. Dorsomedial frontal area 9 tracked others’ performances, but also integrated contextual and self-related information. Self-other mergence increased with the strength of self and other representations in area 9, suggesting it carries interdependent representations of self and other.

Objects tell us what action we can expect: Dissociating brain areas for retrieval and exploitation of action knowledge during action observation in fMRI

Objects are reminiscent of actions often performed with them: knife and apple remind us on peeling the apple or cutting it. Mnemonic representations of object-related actions (action codes) evoked by the sight of an object may constrain and hence facilitate recognition of unrolling actions. The present fMRI study investigated if and how action codes influence brain activation during action observation. The average number of action codes (NAC) of 51 sets of objects was rated by a group of n = 24 participants. In an fMRI study, different volunteers were asked to recognize actions performed with the same objects presented in short videos. To disentangle areas reflecting the storage of action codes from those exploiting them, we showed object-compatible and object-incompatible (pantomime) actions. Areas storing action codes were considered to positively co-vary with NAC in both object-compatible and object-incompatible action; due to its role in tool-related tasks, we here hypothesized left anterior inferior parietal cortex (aIPL). In contrast, areas exploiting action codes were expected to show this correlation only in object-compatible but not incompatible action, as only object-compatible actions match one of the active action codes. For this interaction, we hypothesized ventrolateral premotor cortex (PMv) to join aIPL due to its role in biasing competition in IPL. We found left anterior intraparietal sulcus (IPS) and left posterior middle temporal gyrus (pMTG) to co-vary with NAC. In addition to these areas, action codes increased activity in object-compatible action in bilateral PMv, right IPS, and lateral occipital cortex (LO). Findings suggest that during action observation, the brain derives possible actions from perceived objects, and uses this information to shape action recognition. In particular, the number of expectable actions quantifies the activity level at PMv, IPL, and pMTG, but only PMv reflects their biased competition while observed action unfolds.

Interplay Between Conceptual Expectations and Movement Predictions Underlies Action Understanding

Recent accounts of understanding goal-directed action underline the importance of a hierarchical predictive architecture. However, the neural implementation of such an architecture remains elusive. In the present study, we used functional neuroimaging to quantify brain activity associated with predicting physical movements, as they were modulated by conceptual-expectations regarding the purpose of the object involved in the action. Participants observed object-related actions preceded by a cue that generated both conceptual goal expectations and movement goal predictions. In 2 tasks, observers judged whether conceptual or movement goals matched or mismatched the cue. At the conceptual level, expected goals specifically recruited the posterior cingulate cortex, irrespectively of the task and the perceived movement goal. At the movement level, neural activation of the parieto-frontal circuit, including inferior frontal gyrus and the inferior parietal lobe, reflected unpredicted movement goals. Crucially, this movement prediction error was only present when the purpose of the involved object was expected. These findings provide neural evidence that prior conceptual expectations influence processing of physical movement goals and thereby support the hierarchical predictive account of action processing.

Simultaneous representation of a spectrum of dynamically changing value estimates during decision making.

Decisions are based on value expectations derived from experience. We show that dorsal anterior cingulate cortex and three other brain regions hold multiple representations of choice value based on different timescales of experience organized in terms of systematic gradients across the cortex. Some parts of each area represent value estimates based on recent reward experience while others represent value estimates based on experience over the longer term. The value estimates within these areas interact with one another according to their temporal scaling. Some aspects of the representations change dynamically as the environment changes. The spectrum of value estimates may act as a flexible selection mechanism for combining experience-derived value information with other aspects of value to allow flexible and adaptive decisions in changing environments.Activity in dorsal anterior cingulate cortex (dACC) dynamically tracks the value of the choice after every outcome. Here the authors report that dACC represents topographic maps of value estimates for different learning rates and interacts with similar maps in other areas at the time of the decision.

Olfactory Sensor Processing in Neural Networks: Lessons from Modeling the Fruit Fly Antennal Lobe

The insect olfactory system can be a model for artificial olfactory devices. In particular, Drosophila melanogaster due to its genetic tractability has yielded much information about the design and function of such systems in biology. In this study we investigate possible network topologies to separate representations of odors in the primary olfactory neuropil, the antennal lobe. In particular we compare networks based on stochastic and homogeneous connection weight distributions to connectivities that are based on the input correlations between the glomeruli in the antennal lobe. We show that moderate homogeneous inhibition implements a soft winner-take-all mechanism when paired with realistic input from a large meta-database of odor responses in receptor cells (DoOR database). The sparseness of representations increases with stronger inhibition. Excitation, on the other hand, pushes the representation of odors closer together thus making them harder to distinguish. We further analyze the relationship between different inhibitory network topologies and the properties of the receptor responses to different odors. We show that realistic input from the DoOR database has a relatively high entropy of activation values over all odors and receptors compared to the theoretical maximum. Furthermore, under conditions in which the information in the input is artificially decreased, networks with heterogeneous topologies based on the similarity of glomerular response profiles perform best. These results indicate that in order to arrive at the most beneficial representation for odor discrimination it is important to finely tune the strength of inhibition in combination with taking into account the properties of the available sensors.

Inverted activity patterns in ventromedial prefrontal cortex during value-guided decision-making in a less-is-more task

Ventromedial prefrontal cortex has been linked to choice evaluation and decision-making in humans but understanding the role it plays is complicated by the fact that little is known about the corresponding area of the macaque brain. We recorded activity in macaques using functional magnetic resonance imaging during two very different value-guided decision-making tasks. In both cases ventromedial prefrontal cortex activity reflected subjective choice values during decision-making just as in humans but the relationship between the blood oxygen level-dependent signal and both decision-making and choice value was inverted and opposite to the relationship seen in humans. In order to test whether the ventromedial prefrontal cortex activity related to choice values is important for decision-making we conducted an additional lesion experiment; lesions that included the same ventromedial prefrontal cortex region disrupted normal subjective evaluation of choices during decision-making.Ventromedial prefrontal cortex in humans shows functional magnetic resonance imaging signals related to the subjective values of choices that are taken during decision-making as well as task-negative signals. Here, the authors report that in macaque ventromedial prefrontal cortex both activity patterns are inverted and lesions of this area disrupt subjective choice evaluation.