Conversion of object identity to object-general semantic value in the primate temporal cortex

Keita Tamura , Masaki Takeda, Rieko Setsuie, Tadashi Tsubota, Toshiyuki Hirabayashi, Kentaro Miyamoto, Yasushi Miyashita
Science  18 Aug 2017: Vol. 357, Issue 6352, pp. 687-692

At the final stage of the ventral visual stream, perirhinal neurons encode the identity of memorized objects through learning. However, it remains elusive whether and how object percepts alone, or concomitantly a nonphysical attribute of the objects (“learned”), are decoded from perirhinal activities. By combining monkey psychophysics with optogenetic and electrical stimulations, we found a focal spot of memory neurons where both stimulations led monkeys to preferentially judge presented objects as “already seen.” In an adjacent fringe area, where neurons did not exhibit selective responses to the learned objects, electrical stimulation induced the opposite behavioral bias toward “never seen before,” whereas optogenetic stimulation still induced bias toward “already seen.” These results suggest that mnemonic judgment of objects emerges via the decoding of their nonphysical attributes encoded by perirhinal neurons.


Piercing of Consciousness as a Threshold-Crossing Operation

Yul H.R. Kang, Frederike H. Petzschner, Daniel M. Wolpert, Michael N. Shadlen
Current Biology, Volume 27, Issue 15, p2285–2295.e6, 7 August 2017

Many decisions arise through an accumulation of evidence to a terminating threshold. The process, termed bounded evidence accumulation (or drift diffusion), provides a unified account of decision speed and accuracy, and it is supported by neurophysiology in human and animal models. In many situations, a decision maker may not communicate a decision immediately and yet feel that at some point she had made up her mind. We hypothesized that this occurs when an accumulation of evidence reaches a termination threshold, registered, subjectively, as an “aha” moment. We asked human participants to make perceptual decisions about the net direction of dynamic random dot motion. The difficulty and viewing duration were controlled by the experimenter. After indicating their choice, participants adjusted the setting of a clock to the moment they felt they had reached a decision. The subjective decision times (tSDs) were faster on trials with stronger (easier) motion, and they were well fit by a bounded drift-diffusion model. The fits to the tSDs alone furnished parameters that fully predicted the choices (accuracy) of four of the five participants. The quality of the prediction provides compelling evidence that these subjective reports correspond to the terminating process of a decision rather than a post hoc inference or arbitrary report. Thus, conscious awareness of having reached a decision appears to arise when the brain’s representation of accumulated evidence reaches a threshold or bound. We propose that such a mechanism might play a more widespread role in the “piercing of consciousness” by non-conscious thought processes.


Selective overweighting of larger magnitudes during noisy numerical comparison

Bernhard Spitzer, Leonhard Waschke & Christopher Summerfield
Nature Human Behaviour 1, Article number: 0145 (2017)

Humans are often required to compare average magnitudes in numerical data; for example, when comparing product prices on two rival consumer websites. However, the neural and computational mechanisms by which numbers are weighted, integrated and compared during categorical decisions are largely unknown1,2,3,4,5. Here, we show a systematic deviation from ‘optimality’ in both visual and auditory tasks requiring averaging of symbolic numbers. Participants comparing numbers drawn from two categories selectively overweighted larger numbers when making a decision, and larger numbers evoked disproportionately stronger decision-related neural signals over the parietal cortex. A representational similarity analysis6 showed that neural (dis)similarity in patterns of electroencephalogram activity reflected numerical distance, but that encoding of number in neural data was systematically distorted in a way predicted by the behavioural weighting profiles, with greater neural distance between adjacent larger numbers. Finally, using a simple computational model, we show that although it is suboptimal for a lossless observer, this selective overweighting policy paradoxically maximizes expected accuracy by making decisions more robust to noise arising during approximate numerical integration2. In other words, although selective overweighting discards decision information, it can be beneficial for limited-capacity agents engaging in rapid numerical averaging.


Functional dissection of signal and noise in MT and LIP during decision-making

Jacob L Yates, Il Memming Park, Leor N Katz, Jonathan W Pillow & Alexander C Huk
Nature Neuroscience (2017) doi:10.1038/nn.4611

During perceptual decision-making, responses in the middle temporal (MT) and lateral intraparietal (LIP) areas appear to map onto theoretically defined quantities, with MT representing instantaneous motion evidence and LIP reflecting the accumulated evidence. However, several aspects of the transformation between the two areas have not been empirically tested. We therefore performed multistage systems identification analyses of the simultaneous activity of MT and LIP during individual decisions. We found that monkeys based their choices on evidence presented in early epochs of the motion stimulus and that substantial early weighting of motion was present in MT responses. LIP responses recapitulated MT early weighting and contained a choice-dependent buildup that was distinguishable from motion integration. Furthermore, trial-by-trial variability in LIP did not depend on MT activity. These results identify important deviations from idealizations of MT and LIP and motivate inquiry into sensorimotor computations that may intervene between MT and LIP.


Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment

Anthony Burgos-Robles, Eyal Y Kimchi, Ehsan M Izadmehr, Mary Jane Porzenheim, William A Ramos-Guasp, Edward H Nieh, Ada C Felix-Ortiz, Praneeth Namburi, Christopher A Leppla, Kara N Presbrey, Kavitha K Anandalingam, Pablo A Pagan-Rivera, Melodi Anahtar, Anna Beyeler & Kay M Tye
Nature Neuroscience 20, 824–835 (2017)

Orchestrating appropriate behavioral responses in the face of competing signals that predict either rewards or threats in the environment is crucial for survival. The basolateral nucleus of the amygdala (BLA) and prelimbic (PL) medial prefrontal cortex have been implicated in reward-seeking and fear-related responses, but how information flows between these reciprocally connected structures to coordinate behavior is unknown. We recorded neuronal activity from the BLA and PL while rats performed a task wherein competing shock- and sucrose-predictive cues were simultaneously presented. The correlated firing primarily displayed a BLAright arrowPL directionality during the shock-associated cue. Furthermore, BLA neurons optogenetically identified as projecting to PL more accurately predicted behavioral responses during competition than unidentified BLA neurons. Finally photostimulation of the BLAright arrowPL projection increased freezing, whereas both chemogenetic and optogenetic inhibition reduced freezing. Therefore, the BLAright arrowPL circuit is critical in governing the selection of behavioral responses in the face of competing signals.


Manipulating fear associations via optogenetic modulation of amygdala inputs to prefrontal cortex

Oded Klavir, Matthias Prigge, Ayelet Sarel, Rony Paz & Ofer Yizhar
Nature Neuroscience 20, 836–844 (2017)

Fear-related disorders are thought to reflect strong and persistent fear memories. The basolateral amygdala (BLA) and the medial prefrontal cortex (mPFC) form strong reciprocal synaptic connections that play a key role in acquisition and extinction of fear memories. While synaptic contacts of BLA cells onto mPFC neurons are likely to play a crucial role in this process, the BLA connects with several additional nuclei within the fear circuit that could relay fear-associated information to the mPFC, and the contribution of direct monosynaptic BLA–mPFC inputs is not yet clear. Here we establish an optogenetic stimulation protocol that induces synaptic depression in BLA–mPFC synapses. In behaving mice, optogenetic high-frequency stimulation of BLA inputs to mPFC interfered with retention of cued associations, attenuated previously acquired cue-associated responses in mPFC neurons and facilitated extinction. Our findings demonstrate the contribution of BLA inputs to mPFC in forming and maintaining cued fear associations.


The neural correlates of dreaming

Francesca Siclari, Benjamin Baird, Lampros Perogamvros, Giulio Bernardi, Joshua J LaRocque, Brady Riedner, Melanie Boly, Bradley R Postle & Giulio Tononi
Nature Neuroscience 20, 872–878 (2017)

Consciousness never fades during waking. However, when awakened from sleep, we sometimes recall dreams and sometimes recall no experiences. Traditionally, dreaming has been identified with rapid eye-movement (REM) sleep, characterized by wake-like, globally 'activated', high-frequency electroencephalographic activity. However, dreaming also occurs in non-REM (NREM) sleep, characterized by prominent low-frequency activity. This challenges our understanding of the neural correlates of conscious experiences in sleep. Using high-density electroencephalography, we contrasted the presence and absence of dreaming in NREM and REM sleep. In both NREM and REM sleep, reports of dream experience were associated with local decreases in low-frequency activity in posterior cortical regions. High-frequency activity in these regions correlated with specific dream contents. Monitoring this posterior 'hot zone' in real time predicted whether an individual reported dreaming or the absence of dream experiences during NREM sleep, suggesting that it may constitute a core correlate of conscious experiences in sleep.


Dynamic hidden states underlying working-memory-guided behavior

Michael J Wolff, Janina Jochim, Elkan G Akyürek & Mark G Stokes
Nature Neuroscience 20, 864–871 (2017)

Recent theoretical models propose that working memory is mediated by rapid transitions in 'activity-silent' neural states (for example, short-term synaptic plasticity). According to the dynamic coding framework, such hidden state transitions flexibly configure memory networks for memory-guided behavior and dissolve them equally fast to allow forgetting. We developed a perturbation approach to measure mnemonic hidden states in an electroencephalogram. By 'pinging' the brain during maintenance, we show that memory-item-specific information is decodable from the impulse response, even in the absence of attention and lingering delay activity. Moreover, hidden memories are remarkably flexible: an instruction cue that directs people to forget one item is sufficient to wipe the corresponding trace from the hidden state. In contrast, temporarily unattended items remain robustly coded in the hidden state, decoupling attentional focus from cue-directed forgetting. Finally, the strength of hidden-state coding predicts the accuracy of working-memory-guided behavior, including memory precision.


Moral transgressions corrupt neural representations of value

Molly J Crockett, Jenifer Z Siegel, Zeb Kurth-Nelson, Peter Dayan & Raymond J Dolan
Nature Neuroscience 20, 879–885 (2017)

Moral systems universally prohibit harming others for personal gain. However, we know little about how such principles guide moral behavior. Using a task that assesses the financial cost participants ascribe to harming others versus themselves, we probed the relationship between moral behavior and neural representations of profit and pain. Most participants displayed moral preferences, placing a higher cost on harming others than themselves. Moral preferences correlated with neural responses to profit, where participants with stronger moral preferences had lower dorsal striatal responses to profit gained from harming others. Lateral prefrontal cortex encoded profit gained from harming others, but not self, and tracked the blameworthiness of harmful choices. Moral decisions also modulated functional connectivity between lateral prefrontal cortex and the profit-sensitive region of dorsal striatum. The findings suggest moral behavior in our task is linked to a neural devaluation of reward realized by a prefrontal modulation of striatal value representations.


Posterior Parietal Cortex Guides Visual Decisions in Rats

Angela M. Licata, Matthew T. Kaufman, David Raposo, Michael B. Ryan, John P. Sheppard and Anne K. Churchland
Journal of Neuroscience 13 April 2017, 37 (19) 4954-4966

Neurons in putative decision-making structures can reflect both sensory and decision signals, making their causal role in decisions unclear. Here, we tested whether rat posterior parietal cortex (PPC) is causal for processing visual sensory signals or instead for accumulating evidence for decision alternatives. We disrupted PPC activity optogenetically during decision making and compared effects on decisions guided by auditory versus visual evidence. Deficits were largely restricted to visual decisions. To further test for visual dominance in PPC, we evaluated electrophysiological responses after individual sensory events and observed much larger response modulation after visual stimuli than auditory stimuli. Finally, we measured trial-to-trial spike count variability during stimulus presentation and decision formation. Variability decreased sharply, suggesting that the network is stabilized by inputs, unlike what would be expected if sensory signals were locally accumulated. Our findings suggest that PPC plays a causal role in processing visual signals that are accumulated elsewhere.