Neural ensemble dynamics underlying a long-term associative memory

Grewe BF, Gründemann J, Kitch LJ, Lecoq JA, Parker JG, Marshall JD, Larkin MC, Jercog PE, Grenier F, Li JZ, Lüthi A, Schnitzer MJ
Nature. 2017 Mar 30;543(7647):670-675. doi: 10.1038/nature21682. Epub 2017 Mar 22.

The brain's ability to associate different stimuli is vital for long-term memory, but how neural ensembles encode associative memories is unknown. Here we studied how cell ensembles in the basal and lateral amygdala encode associations between conditioned and unconditioned stimuli (CS and US, respectively). Using a miniature fluorescence microscope, we tracked the Ca2+ dynamics of ensembles of amygdalar neurons during fear learning and extinction over 6 days in behaving mice. Fear conditioning induced both up- and down-regulation of individual cells' CS-evoked responses. This bi-directional plasticity mainly occurred after conditioning, and reshaped the neural ensemble representation of the CS to become more similar to the US representation. During extinction training with repetitive CS presentations, the CS representation became more distinctive without reverting to its original form. Throughout the experiments, the strength of the ensemble-encoded CS-US association predicted the level of behavioural conditioning in each mouse. These findings support a supervised learning model in which activation of the US representation guides the transformation of the CS representation.


Nonpolitical Images Evoke Neural Predictors of Political Ideology

Woo-Young Ahn, Kenneth T. Kishida, Xiaosi Gu, Terry Lohrenz, Ann Harvey, John R. Alford, Kevin B. Smith, Gideon Yaffe, John R. Hibbing, Peter Dayan, P. Read Montague
Current Biology. Volume 24, Issue 22, p2693–2699, 17 November 2014

Political ideologies summarize dimensions of life that define how a person organizes their public and private behavior, including their attitudes associated with sex, family, education, and personal autonomy [ 1, 2 ]. Despite the abstract nature of such sensibilities, fundamental features of political ideology have been found to be deeply connected to basic biological mechanisms [ 3–7 ] that may serve to defend against environmental challenges like contamination and physical threat [ 8–12 ]. These results invite the provocative claim that neural responses to nonpolitical stimuli (like contaminated food or physical threats) should be highly predictive of abstract political opinions (like attitudes toward gun control and abortion) [ 13 ]. We applied a machine-learning method to fMRI data to test the hypotheses that brain responses to emotionally evocative images predict individual scores on a standard political ideology assay. Disgusting images, especially those related to animal-reminder disgust (e.g., mutilated body), generate neural responses that are highly predictive of political orientation even though these neural predictors do not agree with participants’ conscious rating of the stimuli. Images from other affective categories do not support such predictions. Remarkably, brain responses to a single disgusting stimulus were sufficient to make accurate predictions about an individual subject’s political ideology. These results provide strong support for the idea that fundamental neural processing differences that emerge under the challenge of emotionally evocative stimuli may serve to structure political beliefs in ways formerly unappreciated.


How prior preferences determine decision-making frames and biases in the human brain

Lopez-Persem A, Domenech P, Pessiglione M
Elife. 2016 Nov 19;5. pii: e20317. doi: 10.7554/eLife.20317.

Understanding how option values are compared when making a choice is a key objective for decision neuroscience. In natural situations, agents may have a priori on their preferences that create default policies and shape the neural comparison process. We asked participants to make choices between items belonging to different categories (e.g., jazz vs. rock music). Behavioral data confirmed that the items taken from the preferred category were chosen more often and more rapidly, which qualified them as default options. FMRI data showed that baseline activity in classical brain valuation regions, such as the ventromedial Prefrontal Cortex (vmPFC), reflected the strength of prior preferences. In addition, evoked activity in the same regions scaled with the default option value, irrespective of the eventual choice. We therefore suggest that in the brain valuation system, choices are framed as comparisons between default and alternative options, which might save some resource but induce a decision bias.


Dynamic neural architecture for social knowledge retrieval

Y Wang et al.
Proc Natl Acad Sci U S A 114 (16), E3305-E3314. 2017 Mar 13.

Social behavior is often shaped by the rich storehouse of biographical information that we hold for other people. In our daily life, we rapidly and flexibly retrieve a host of biographical details about individuals in our social network, which often guide our decisions as we navigate complex social interactions. Even abstract traits associated with an individual, such as their political affiliation, can cue a rich cascade of person-specific knowledge. Here, we asked whether the anterior temporal lobe (ATL) serves as a hub for a distributed neural circuit that represents person knowledge. Fifty participants across two studies learned biographical information about fictitious people in a 2-d training paradigm. On day 3, they retrieved this biographical information while undergoing an fMRI scan. A series of multivariate and connectivity analyses suggest that the ATL stores abstract person identity representations. Moreover, this region coordinates interactions with a distributed network to support the flexible retrieval of person attributes. Together, our results suggest that the ATL is a central hub for representing and retrieving person knowledge.


Neural processes mediating contextual influences on human choice behaviour

Francesco Rigoli, Karl J. Friston & Raymond J. Dolan
Nature Communications 7, Article number: 12416 (2016) doi:10.1038/ncomms12416

Contextual influences on choice are ubiquitous in ecological settings. Current evidence suggests that subjective values are normalized with respect to the distribution of potentially available rewards. However, how this context-sensitivity is realised in the brain remains unknown. To address this, here we examine functional magnetic resonance imaging (fMRI) data during performance of a gambling task where blocks comprise values drawn from one of two different, but partially overlapping, reward distributions or contexts. At the beginning of each block (when information about context is provided), hippocampus is activated and this response is enhanced when contextual influence on choice increases. In addition, response to value in ventral tegmental area/substantia nigra (VTA/SN) shows context-sensitivity, an effect enhanced with an increased contextual influence on choice. Finally, greater response in hippocampus at block start is associated with enhanced context sensitivity in VTA/SN. These findings suggest that context-sensitive choice is driven by a brain circuit involving hippocampus and dopaminergic midbrain.


Confidence Is the Bridge between Multi-stage Decisions

van den Berg R, Zylberberg A, Kiani R, Shadlen MN, Wolpert DM
Curr Biol. 2016 Dec 5;26(23):3157-3168. doi: 10.1016/j.cub.2016.10.021.

Demanding tasks often require a series of decisions to reach a goal. Recent progress in perceptual decision-making has served to unite decision accuracy, speed, and confidence in a common framework of bounded evidence accumulation, furnishing a platform for the study of such multi-stage decisions. In many instances, the strategy applied to each decision, such as the speed-accuracy trade-off, ought to depend on the accuracy of the previous decisions. However, as the accuracy of each decision is often unknown to the decision maker, we hypothesized that subjects may carry forward a level of confidence in previous decisions to affect subsequent decisions. Subjects made two perceptual decisions sequentially and were rewarded only if they made both correctly. The speed and accuracy of individual decisions were explained by noisy evidence accumulation to a terminating bound. We found that subjects adjusted their speed-accuracy setting by elevating the termination bound on the second decision in proportion to their confidence in the first. The findings reveal a novel role for confidence and a degree of flexibility, hitherto unknown, in the brain's ability to rapidly and precisely modify the mechanisms that control the termination of a decision.


Observational learning computations in neurons of the human anterior cingulate cortex

Michael R. Hill, Erie D. Boorman & Itzhak Fried
Nature Communications 7, Article number: 12722 (2016) doi:10.1038/ncomms12722

When learning from direct experience, neurons in the primate brain have been shown to encode a teaching signal used by algorithms in artificial intelligence: the reward prediction error (PE)—the difference between how rewarding an event is, and how rewarding it was expected to be. However, in humans and other species learning often takes place by observing other individuals. Here, we show that, when humans observe other players in a card game, neurons in their rostral anterior cingulate cortex (rACC) encode both the expected value of an observed choice, and the PE after the outcome was revealed. Notably, during the same task neurons recorded in the amygdala (AMY) and the rostromedial prefrontal cortex (rmPFC) do not exhibit this type of encoding. Our results suggest that humans learn by observing others, at least in part through the encoding of observational PEs in single neurons in the rACC.