Ilya E. Monosov’s research while affiliated with Washington and Lee University and other places

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Publications (43)


Fig. 2. A) Alpha coherence (8 to 15 Hz) differences between the high and low arousal state across region-pairs. Each colored box represents the average alpha coherence difference between the two arousal states (high-low arousal) for the indicated region-pair (labels on left and bottom of matrix). Blue colors indicate coherence increases during low arousal epochs when compared to high arousal epochs. Red colors indicate coherence increases during high arousal epochs when compared to low arousal epochs. Most regions showed broad increases in alpha coherence during low arousal epochs. However, medial temporal areas that include entorhinal cortex, medial temporal cortex, and hippocampus did not show this global increase in coherence during low arousal epochs (each of these regions is labeled with a different hue of green). The boxed inset shows alpha and gamma coherence across all region-pairs during the first 15 s of low arousal, last 15 s of low arousal, and first 15 s of high arousal (left-to-right). Global alpha coherence is greater at the beginning compared to the end of low arousal, while global gamma coherence does not change from the beginning to end of low arousal (P < 0.001 and P = 0.27, respectively, Wilcoxon signed-rank test). Global alpha coherence decreases further from the end of low arousal to the beginning of high arousal, while global gamma coherence increases from the end of low arousal to the beginning of high arousal (P < 0.001, Wilcoxon signed-rank test). B) Comparison of alpha coherence during high and low arousal states across regions. Average alpha coherence during high (y-axis) and low (x-axis) arousal is represented as a black circle for an individual region, with lines indicating standard error. Equal alpha coherence between arousal states is represented by the dashed red line (identity line, x = y). Medial temporal regions are exclusively above the identity line (green hues indicate specific regions). The boxed inset shows a comparison of alpha power and coherence differences between high and low arousal states for each region, highlighting the specific deviation of arousal-related alpha coherence in medial temporal areas. In this inset, the red dashed line represents no change in alpha power/ coherence between arousal states, the green-hued dots represent specific medial temporal areas, and gray dots represent all other regions. C) Coherence difference between high and low arousal states for each region at alpha, beta, and gamma frequencies. For each frequency band, a black dot represents the average coherence difference between arousal states (high-low arousal epochs) for that region with every other region with vertical lines indicating standard error. Green hues label specific medial temporal regions. 9/46D, dorsal pallidum, 9/46V, 6, 8d, OFC, 3ab, striatum, 45B/8v, insula, and basal forebrain increased alpha coherence on average during low arousal epochs (one-sample t-test, Bonferroni multiple comparisons correction, corrected P < 0.001). Anterior-ventral medial temporal cortex, hippocampus, anterior entorhinal cortex, and posterior-ventral medial temporal cortex all decreased alpha coherence on average during low arousal epochs (one-sample t-test, Bonferroni multiple comparisons correction, corrected P < 0.001). Probability density functions (right panel) show distribution of average coherence difference across regions. No visible relationship was seen between distributions in alpha coherence differences and distributions in beta/gamma coherence differences. D) Spring-embedded graph network for visualization of alpha coherence during high and low arousal states. Each blue line represents a weighted edge of the network and indicates a coherence value >0.2 while every black dot marks a node in the network, representing a specific region.
Arousal effects on oscillatory dynamics in the non-human primate brain
  • Article
  • Full-text available

December 2024

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13 Reads

Cerebral Cortex

Shashank A Anand

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Fatih Sogukpinar

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Ilya E Monosov

Arousal states are thought to influence many aspects of cognition and behavior by broadly modulating neural activity. Many studies have observed arousal-related modulations of alpha (~8 to 15 Hz) and gamma (~30 to 50 Hz) power and coherence in local field potentials across relatively small groups of brain regions. However, the global pattern of arousal-related oscillatory modulation in local field potentials is yet to be fully elucidated. We simultaneously recorded local field potentials in numerous cortical and subcortical regions in the primate brain and assessed oscillatory activity and inter-regional coherence associated with arousal state. In high arousal states, we found a uniquely strong and coherent gamma oscillation between the amygdala and basal forebrain. In low arousal rest-like states, a relative increase in coherence at alpha frequencies was present across sampled brain regions, with the notable exception of the medial temporal lobe. We consider how these patterns of activity may index arousal-related brain states that support the processing of incoming sensory stimuli during high arousal states and memory-related functions during rest.

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Curiosity: primate neural circuits for novelty and information seeking

January 2024

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118 Reads

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11 Citations

Nature Reviews Neuroscience

For many years, neuroscientists have investigated the behavioural, computational and neurobiological mechanisms that support value-based decisions, revealing how humans and animals make choices to obtain rewards. However, many decisions are influenced by factors other than the value of physical rewards or second-order reinforcers (such as money). For instance, animals (including humans) frequently explore novel objects that have no intrinsic value solely because they are novel and they exhibit the desire to gain information to reduce their uncertainties about the future, even if this information cannot lead to reward or assist them in accomplishing upcoming tasks. In this Review, I discuss how circuits in the primate brain responsible for detecting, predicting and assessing novelty and uncertainty regulate behaviour and give rise to these behavioural components of curiosity. I also briefly discuss how curiosity-related behaviours arise during postnatal development and point out some important reasons for the persistence of curiosity across generations.


A neural mechanism for conserved value computations integrating information and rewards

January 2024

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179 Reads

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17 Citations

Nature Neuroscience

Behavioral and economic theory dictate that we decide between options based on their values. However, humans and animals eagerly seek information about uncertain future rewards, even when this does not provide any objective value. This implies that decisions are made by endowing information with subjective value and integrating it with the value of extrinsic rewards, but the mechanism is unknown. Here, we show that human and monkey value judgements obey strikingly conserved computational principles during multi-attribute decisions trading off information and extrinsic reward. We then identify a neural substrate in a highly conserved ancient structure, the lateral habenula (LHb). LHb neurons signal subjective value, integrating information’s value with extrinsic rewards, and the LHb predicts and causally influences ongoing decisions. Neurons in key input areas to the LHb largely signal components of these computations, not integrated value signals. Thus, our data uncover neural mechanisms of conserved computations underlying decisions to seek information about the future.


Dorsal raphe neurons signal integrated value during multi-attribute decision-making

August 2023

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49 Reads

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3 Citations

The dorsal raphe nucleus (DRN) is implicated in psychiatric disorders that feature impaired sensitivity to reward amount, impulsivity when facing reward delays, and risk-seeking when grappling with reward uncertainty. However, whether and how DRN neurons signal reward amount, reward delay, and reward uncertainty during multi-attribute value-based decision-making, where subjects consider all these attributes to make a choice, is unclear. We recorded DRN neurons as monkeys chose between offers whose attributes, namely expected reward amount, reward delay, and reward uncertainty, varied independently. Many DRN neurons signaled offer attributes. Remarkably, these neurons commonly integrated offer attributes in a manner that reflected monkeys' overall preferences for amount, delay, and uncertainty. After decision-making, in response to post-decision feedback, these same neurons signaled signed reward prediction errors, suggesting a broader role in tracking value across task epochs and behavioral contexts. Our data illustrate how DRN participates in integrated value computations, guiding theories of DRN in decision-making and psychiatric disease.


A response to claims of emergent intelligence and sentience in a dish

March 2023

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424 Reads

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14 Citations

Neuron

The article ‘In vitro neurons learn and exhibit sentience when embodied in a simulated game-world’ by Kagan et al.1 triggered a wave of positive mainstream and scientific media coverage as well as a widespread negative reaction from the scientific community. Here, we discuss why this negative reaction is legitimate and must be taken seriously. We raise concerns about the key claim of the article: that it demonstrates that “a single layer of in vitro cortical neurons can self-organize activity to display intelligent and sentient behavior when embodied in a simulated game-world”.


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The zona incerta in control of novelty seeking and investigation across species

December 2022

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128 Reads

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14 Citations

Current Opinion in Neurobiology

Many organisms rely on a capacity to rapidly replicate, disperse, and evolve when faced with uncertainty and novelty. But mammals do not evolve and replicate quickly. They rely on a sophisticated nervous system to generate predictions and select responses when confronted with these challenges. An important component of their behavioral repertoire is the adaptive context-dependent seeking or avoiding of perceptually novel objects, even when their values have not yet been learned. Here, we outline recent cross-species breakthroughs that shed light on how the zona incerta (ZI), a relatively evolutionarily conserved brain area, supports novelty-seeking and novelty-related investigations. We then conjecture how the architecture of the ZI's anatomical connectivity – the wide-ranging top-down cortical inputs to the ZI, and its specifically strong outputs to both the brainstem action controllers and to brain areas involved in action value learning – place the ZI in a unique role at the intersection of cognitive control and learning.


Dopamine in the rodent tail of striatum regulates behavioral variability in response to threatening novel objects

November 2022

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15 Reads

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2 Citations

Neuron

Mice display variability in fear-like responses to many external salient events, such as encountering unexpected novel objects, but the neural basis of this variability has been unclear. Akiti et al. (2022) demonstrate that dopamine in the tail of the rodent striatum predicts and regulates salience-related variability in individuals’ behavioral responses to unexpected novel objects.


Some opportunities and limitations of different methods of aversive stimulus delivery
Laser stimulation of the skin for quantitative study of decision-making and motivation

September 2022

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41 Reads

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3 Citations

Cell Reports Methods

Neuroeconomics studies how decision-making is guided by the value of rewards and punishments. But to date, little is known about how noxious experiences impact decisions. A challenge is the lack of an aversive stimulus that is dynamically adjustable in intensity and location, readily usable over many trials in a single experimental session, and compatible with multiple ways to measure neuronal activity. We show that skin laser stimulation used in human studies of aversion can be used for this purpose in several key animal models. We then use laser stimulation to study how neurons in the orbitofrontal cortex (OFC), an area whose many roles include guiding decisions among different rewards, encode the value of rewards and punishments. We show that some OFC neurons integrated the positive value of rewards with the negative value of aversive laser stimulation, suggesting that the OFC can play a role in more complex choices than previously appreciated.


Citations (38)


... Merging ideas from reinforcement learning theory 6 with recent insights into the filtering properties of the dorsal raphe nucleus 7 , here we find a unifying perspective in a prospective code for value. This biological code for near-future reward explains why serotonin neurons are activated by both rewards and punishments 3,4,[8][9][10][11][12][13] , and why these neurons are more strongly activated by surprising rewards but have no such surprise preference for punishments 3,9 -observations that previous theories have failed to reconcile. Finally, our model quantitatively predicts in vivo population activity better than previous theories. ...

Reference:

A prospective code for value in the serotonin system
Dorsal raphe neurons integrate the values of reward amount, delay, and uncertainty in multi-attribute decision-making
  • Citing Article
  • June 2024

Cell Reports

... Risk-coding neurons might respond to different, separately cued reward components and update their risk signal once new information is presented. Although neuronal risk signals have been reported in various brain systems 14,15,22,24,27,[33][34][35][36][37] , how they derive from separately cued attributes is unclear. ...

Curiosity: primate neural circuits for novelty and information seeking
  • Citing Article
  • January 2024

Nature Reviews Neuroscience

... In addition, metabolic systems flexibly allocate resources towards processes such as organ growth and immune response to infection depending on the metabolome [5,6,7]. Those observations have motivated biologists to elucidate how organisms optimally integrate and/or select information sources from the exposome in an ever-changing world [8,9,10,11]. ...

A neural mechanism for conserved value computations integrating information and rewards

Nature Neuroscience

... ; https://doi.org/10.1101/2023.09.19.558526 doi: bioRxiv preprint tation from a bottom-up model of the DRN (10). Neither of these are new to the serotonin field (14,43,44,(74)(75)(76)(77)(78)(79)(80), but, to the best of our knowledge, they have not previously been combined. The fact that serotonergic responses to rewards and punishments only become interpretable after accounting for the effects of adaptation illustrates the usefulness of elements of biological detail even in normatively-focused branches of computational neuroscience. ...

Dorsal raphe neurons signal integrated value during multi-attribute decision-making

... This was a rationale for delivering unpredictable noise to the sensory electrodes of the cell culture (or restarting the game in an unpredictable way), whenever the neuronal network failed to hit the ball (Kagan et al., 2022). Some found the results reported in Kagan et al. (2022) remarkable, but not in a good way: they disagreed with the claim that the behavior could be described as "sentient" (Balci et al., 2023). Here, we hope to make sense of the notion of sentient behavior in terms of Bayesian belief updating, where "sentient behavior" denotes the capacity to generate appropriate responses to sensory perturbations (as opposed to merely reactive behavior; Kagan, Razi et al., 2023). ...

A response to claims of emergent intelligence and sentience in a dish

Neuron

... Several neocortical and subcortical areas, including the prefrontal cortex, zona incerta, amygdala, and striatum, have been identified as critical nodes in the circuitry supporting novelty exploration in the context of both novel item exploration and explore-exploit decision-making [7,42,48,49]. A small number of studies have also pointed to roles for the hippocampus and dentate gyrus in novelty exploration [7,28,50,55]. ...

The zona incerta in control of novelty seeking and investigation across species

Current Opinion in Neurobiology

... A recent preprint reports a possible site for such integration in the macaque brain. In a decision-making task involving a trade-off between information and reward, neurons in the lateral habenula combined the value of information and extrinsic reward to signal the subjective value of possible choices using a common code [91]. Moreover, perturbation of neural activity in the lateral habenula biased choice behavior in a manner consistent with reducing subjective value. ...

A neural mechanism for conserved value computations integrating information and rewards

... We define novel stimuli as those with limited or no prior perceptual exposure, whereas familiar stimuli are defined as those that have been experienced extensively (high perceptual exposure). Canonical novelty responses (i.e., higher activation elicited by novel images than familiar ones) have been found across the monkey brain, notably including inferotemporal cortex (IT; Zhang, Bromberg-Martin, Sogukpinar, Kocher, & Monosov, 2022;Ghazizadeh et al., 2020;Huang, Ramachandran, Lee, & Olson, 2018;Ranganath & Rainer, 2003), the superior temporal sulcus (Uhrig, Dehaene, & Jarraya, 2014), and in LPFC (Ghazizadeh & Hikosaka, 2022;Ghazizadeh et al., 2020;Uhrig et al., 2014;Matsumoto, Matsumoto, & Tanaka, 2007;Mruczek & Sheinberg, 2007;Rolls, Browning, Inoue, & Hernadi, 2005). These novelty responses are thought to arise, in part, through a graded change in the neural activity, such that novel stimuli have large, distributed neural representations that gradually shift to smaller, more finely tuned sets of neurons as perceptual exposure increases (Koyano et al., 2023;Rainer & Miller, 2000). ...

Surprise and recency in novelty detection in the primate brain

Current Biology