Tag: neuron level

Neural correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field.

Ding, L. and Gold, J. I.
Cereb Cortex, 22:1052–1067, 2012
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Abstract

Perceptual decision making requires a complex set of computations to implement, evaluate, and adjust the conversion of sensory input into a categorical judgment. Little is known about how the specific underlying computations are distributed across and within different brain regions. Using a reaction-time (RT) motion direction-discrimination task, we show that a unique combination of decision-related signals is represented in monkey frontal eye field (FEF). Some responses were modulated by choice, motion strength, and RT, consistent with a temporal accumulation of sensory evidence. These responses converged to a threshold level prior to behavioral responses, reflecting decision commitment. Other responses continued to be modulated by motion strength even after decision commitment, possibly providing a memory trace to help evaluate and adjust the decision process with respect to rewarding outcomes. Both response types were encoded by FEF neurons with both narrow- and broad-spike waveforms, presumably corresponding to inhibitory interneurons and excitatory pyramidal neurons, respectively, and with diverse visual, visuomotor, and motor properties, albeit with different frequencies. Thus, neurons throughout FEF appear to make multiple contributions to decision making that only partially overlap with contributions from other brain regions. These results help to constrain how networks of brain regions interact to generate perceptual decisions.

Review

This paper puts some perspective in the usually communicated statement that LIP neurons are responsible for perceptual decision making in monkeys who perform a reaction time motion discrimination task. Especially, the authors report on neurons in frontal eye field (FEF) that also show typical accumulation-to-bound responses. Furthermore, at least as many neurons in FEF exhibited activity that was correlated with motion coherence and choice during and after the saccade indicating a choice and extinguishing the stimulus, i.e., the activity of these neurons appeared to accumulate evidence, but seemed to ignore the supposed bound and maintained a representation of the stimulus after it had gone. In the discussion the authors also point to other studies which found activity that can be interpreted in terms of evidence accumulation. Corresponding neurons have been found in LIP, FEF, superior colliculus (SC) and caudate nucleus of which neurons in LIP and SC may be mostly governed by a bound. From the reported and reviewed results it becomes clear that, although accumulation-to-bound may be an important component of perceptual decision making, it is not sufficient to explain the wide variety of decision-related neuronal activity in the brain. In particular, it is unclear how neurons from the mentioned brain regions interact and what their different roles in perceptual decision making are.

Effects of cortical microstimulation on confidence in a perceptual decision.

Fetsch, C. R., Kiani, R., Newsome, W. T., and Shadlen, M. N.
Neuron, 83:797–804, 2014
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Abstract

Decisions are often associated with a degree of certainty, or confidence-an estimate of the probability that the chosen option will be correct. Recent neurophysiological results suggest that the central processing of evidence leading to a perceptual decision also establishes a level of confidence. Here we provide a causal test of this hypothesis by electrically stimulating areas of the visual cortex involved in motion perception. Monkeys discriminated the direction of motion in a noisy display and were sometimes allowed to opt out of the direction choice if their confidence was low. Microstimulation did not reduce overall confidence in the decision but instead altered confidence in a manner that mimicked a change in visual motion, plus a small increase in sensory noise. The results suggest that the same sensory neural signals support choice, reaction time, and confidence in a decision and that artificial manipulation of these signals preserves the quantitative relationship between accumulated evidence and confidence.

Review

The paper provides verification of beliefs asserted in Kiani2009: Confidence is directly linked to accumulated evidence as represented in monkey area LIP during a random dot motion discrimination task. The authors use exactly the same task, but now stimulate patches of MT/MST neurons instead of recording single LIP neurons and resort to analysing behavioural data only. They find that small microstimulation of functionally well-defined neurons, that signal a particular motion direction, affects decisions in the same way as manipulating the motion information in the stimulus directly. This was expected, because it has been shown before that stimulating MT neurons influences decisions in that way. New here is that the effect of stimulation on confidence judgements was evaluated at the same time. The rather humdrum result: confidence judgements are also affected in the same way. The authors argue that this didn’t have to be, because confidence judgements are thought to be a metacognitive process that may be influenced by other high-level cognitive functions such as related to motivation. Then again, isn’t decision making thought to be a high-level cognitive function that is clearly influenced by motivation?

Anyway, there was one small effect particular to stimulation that did not occur in the control experiment where the stimulus itself was manipulated: There was a slight decrease in the overall proportion of sure-bet choices (presumably indicating low confidence) with stimulation suggesting that monkeys were more confident when stimulated. The authors explain this with larger noise (diffusion) in a simple drift-diffusion model. Counterintuitively, the larger accumulation noise increases the probability of moving away from the initial value and out of the low-confidence region. The mechanism makes sense, but I would rather explain it within an equivalent Bayesian model in which MT neurons represent noisy observations that are transformed into noisy pieces of evidence which are accumulated in LIP. Stimulation increases the noise on the observations which in turn increases accumulation noise in the equivalent drift-diffusion model (see Bitzer et al., 2014).

In drift-diffusion models drift, diffusion and threshold are mutually redundant in that one of them needs to be fixed when fitting the model to choices and reaction times. The authors here let all of them vary simultaneously which indicates that the parameters can be discriminated based on confidence judgements even when no reaction time is taken into account. This should be followed up. It is also interesting to think about how the postulated tight link between the ‘decision variable’ and the experienced confidence can be consolidated in a reaction time task where supposedly all decisions are made at the same threshold value. Notice that the confidence of a decision in their framework depends on the state of the diffusion (most likely one of the two boundaries) and the time of the decision: Assuming fixed noise, smaller decision times should translate into larger confidence, because you assume that this is due to a larger drift. Therefore, you should see variability of confidence judgements in a reaction time task that is strongly correlated with reaction times.

Decision-related activity in sensory neurons reflects more than a neuron's causal effect.

Nienborg, H. and Cumming, B. G.
Nature, 459:89–92, 2009
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Abstract

During perceptual decisions, the activity of sensory neurons correlates with a subject’s percept, even when the physical stimulus is identical. The origin of this correlation is unknown. Current theory proposes a causal effect of noise in sensory neurons on perceptual decisions, but the correlation could result from different brain states associated with the perceptual choice (a top-down explanation). These two schemes have very different implications for the role of sensory neurons in forming decisions. Here we use white-noise analysis to measure tuning functions of V2 neurons associated with choice and simultaneously measure how the variation in the stimulus affects the subjects’ (two macaques) perceptual decisions. In causal models, stronger effects of the stimulus upon decisions, mediated by sensory neurons, are associated with stronger choice-related activity. However, we find that over the time course of the trial these measures change in different directions-at odds with causal models. An analysis of the effect of reward size also supports this conclusion. Finally, we find that choice is associated with changes in neuronal gain that are incompatible with causal models. All three results are readily explained if choice is associated with changes in neuronal gain caused by top-down phenomena that closely resemble attention. We conclude that top-down processes contribute to choice-related activity. Thus, even forming simple sensory decisions involves complex interactions between cognitive processes and sensory neurons.

Review

They investigated the source of the choice probability of early sensory neurons. Choice probability quantifies the difference in firing rate distributions separated by the behavioural response of the subject. The less overlap between the firing rate distributions for one response and its alternative (in two-choice tasks), the greater the choice probability. Importantly, they restricted their analysis to trials in which the stimulus was effectively random. In random dot motion experiments this corresponds to 0% coherent motion, but here they used a disparity discrimination task and looked at disparity selective neurons in macaque area V2. The mean contribution from the stimulus, therefore, should have been 0. Yet, they found that choice probability was above 0.5 indicating that the firing of the neurons still could predict the final response, but why? They consider two possibilities: 1) the particular noise in firing rates of sensory neurons causes, at least partially, the final choice. 2) The firing rate of sensory neurons reflects choice-related effects induced by top-down influences from more decision-related areas.

Note that the choice probability they use is somewhat corrected for influences from the stimulus by considering the firing rate of a neuron in response to a particular disparity, but without taking choices into account. This correction reduced choice probabilities a bit. Nevertheless, they remained significantly above 0.5. This result indicates that the firing rate distributions of the recorded neurons were only little affected by which disparities were shown in individual frames when these distributions are defined depending on the final choice. I don’t find this surprising, because there was no consistent stimulus to detect from the random disparities and the behavioural choices were effectively random.

Yet, the particular disparities presented in individual trials had an influence on the final choice. They used psychophysical reverse correlation to determine this. The analysis suggests that the very first frames had a very small effect which is followed by a steep rise in influence of frames at the beginning of a trial (until about 200ms) and then a steady decline. This result can mean different things depending on whether you believe that evidence accumulation stops once you have reached a threshold, or whether evidence accumulation continues until you are required to make a response. Shadlen is probably a proponent of the first proposition. Then, the decreasing influence of the stimulus on the choice just reflects the smaller number of trials in which the threshold hasn’t been reached, yet. Based on the second proposition, the result means that the weight of individual pieces of evidence during accumulation reduces as you come closer to the response. Currently, I can’t think of decisive evidence for either proposition, but it has been shown in perturbation experiments that stimulus perturbations close to a decision, late in a trial had smaller effects on final choices than perturbations early in a trial (Huk and Shadlen, 2005).

Back to the source of above chance-level choice probabilities. The authors argue, given the decreasing influence of the stimulus on the final choice and assuming that the influence of the stimulus on sensory neurons stays constant, that choice probabilities should also decrease towards the end of a trial. However, choice probabilities stay roughly constant after an initial rise. Consequently, they infer that the firing of the neurons must be influenced from other sources, apart from the stimulus, which are correlated with the choice. They consider two of these sources: i) Lateral, sensory neurons which could reflect the final decision better. ii) Higher, decision related areas which, for example, project a kind of bias onto the sensory neurons. The authors strongly prefer ii), also because they found that the firing of sensory neurons appears to be gain modulated when contrasting firing rates between final choices. In particular, firing rates showed a larger gain (steeper disparity tuning curve of neuron) when trials were considered which ended with the behavioural choice corresponding to the preferred dispartiy of the neuron. In other words, the output of a neuron was selectively increased, if that neuron preferred the disparity which was finally chosen. Equivalently, the output of a neuron was selectively decreased, if that neuron preferred a different disparity than the one which was finally chosen. This gain difference explains at least part of the difference in firing rate distributions which the choice probability measures.

They also show an interesting effect of reward size on the correlation between stimulus and final choice: Stimulus had larger influence on choice for larger reward. Again, if the choice probabilities were mainly driven by stimulus, bottom-up related effects and the stimulus had a larger influence on final choice in high reward trials, then choice probabilities should have been higher in high reward trials. The opposite was the case: choice probabilities were lower in high reward trials. The authors explain this using the previous bias hypothesis: The measured choice probabilities reflect something like an attentional gain or bias induced by higher-level decision-related areas. As the stimulus becomes more important, the bias looses influence. Hence, the choice probabilities reduce.

In summary, the authors present convincing evidence that already sensory neurons in early visual cortex (V2) receive top-down, decision-related influences. Compared with a previous paper (Nienborg and Cumming, 2006) the reported choice probabilities here were quite similar to those reported there, even though here only trials with complete random stimuli were considered. I would have guessed that choice probabilities would be considerably higher for trials with an actually presented stimulus. Why is there only a moderate difference? Perhaps there actually isn’t. My observation is only based on a brief look at the figures in the two papers.

The Influence of Spatiotemporal Structure of Noisy Stimuli in Decision Making.

Insabato, A., Dempere-Marco, L., Pannunzi, M., Deco, G., and Romo, R.
PLoS Comput Biol, 10:e1003492, 2014
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Abstract

Decision making is a process of utmost importance in our daily lives, the study of which has been receiving notable attention for decades. Nevertheless, the neural mechanisms underlying decision making are still not fully understood. Computational modeling has revealed itself as a valuable asset to address some of the fundamental questions. Biophysically plausible models, in particular, are useful in bridging the different levels of description that experimental studies provide, from the neural spiking activity recorded at the cellular level to the performance reported at the behavioral level. In this article, we have reviewed some of the recent progress made in the understanding of the neural mechanisms that underlie decision making. We have performed a critical evaluation of the available results and address, from a computational perspective, aspects of both experimentation and modeling that so far have eluded comprehension. To guide the discussion, we have selected a central theme which revolves around the following question: how does the spatiotemporal structure of sensory stimuli affect the perceptual decision-making process? This question is a timely one as several issues that still remain unresolved stem from this central theme. These include: (i) the role of spatiotemporal input fluctuations in perceptual decision making, (ii) how to extend the current results and models derived from two-alternative choice studies to scenarios with multiple competing evidences, and (iii) to establish whether different types of spatiotemporal input fluctuations affect decision-making outcomes in distinctive ways. And although we have restricted our discussion mostly to visual decisions, our main conclusions are arguably generalizable; hence, their possible extension to other sensory modalities is one of the points in our discussion.

Review

They review previous findings about perceptual decision making from a computational perspective, mostly related to attractor models of decision making. The focus here, however, is how the noisy stimulus influences the decision. They mostly restrict themselves to experiments with random dot motion, because these provided most relevant results for their discussion which mainly included three points: 1) specifics of decision input in decisions with multiple alternatives, 2) the relation of the activity of sensory neurons to decisions (cf. CP – choice probability) and 3) in what way sensory neurons reflect fluctuations of the particular stimulus. See also first paragraph of Final Remarks for summary, but note that I have made slightly different points. Their 3rd point derives from mine by applying mine to the specifics of the random dot motion stimuli. In particular, they suggest to investigate in how far different definitions of spatial noise in the random dot stimulus affect decisions differently.

With 2) they discuss the interesting finding that already the activity of sensory neurons can, to some extent, predict final decisions even when the evidence in the stimulus does not favour any decision alternative. So where does the variance in sensory neurons come from which eventually leads to a decision? Obviously, it could come from the stimulus itself. It has been found, however, that the ratio of variance to mean activity is the same when computed over trials with different stimuli compared to when computed over trials in which exactly the same stimulus with a particular realisation of noise was repeated. You would like to see a reduction of variance when the same stimulus is repeated, but it’s not there. I’m unsure, though, whether this is the correct interpretation of the variance-mean-ratio. I would have to check the original papers by Britten (Britten, 1993 and Britten, 1996). The seemingly constant variance of sensory neuron activity suggests that the particular noise realisation of a random dot stimulus does not affect decisions. Rather, the intrinsic activity of sensory neurons drives decisions in the case of no clear evidence. The authors argue that this is not a complete description of the situation, because it has also been found that you can see an effect of the particular stimulus on the variance of sensory neuron activity when considering small time windows instead of the whole trial. Unfortunately, the argument is mostly based on results presented in a SfN meeting abstracts in 2012. I wonder why there is no corresponding paper.

Probabilistic reasoning by neurons.

Yang, T. and Shadlen, M. N.
Nature, 447:1075–1080, 2007
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Abstract

Our brains allow us to reason about alternatives and to make choices that are likely to pay off. Often there is no one correct answer, but instead one that is favoured simply because it is more likely to lead to reward. A variety of probabilistic classification tasks probe the covert strategies that humans use to decide among alternatives based on evidence that bears only probabilistically on outcome. Here we show that rhesus monkeys can also achieve such reasoning. We have trained two monkeys to choose between a pair of coloured targets after viewing four shapes, shown sequentially, that governed the probability that one of the targets would furnish reward. Monkeys learned to combine probabilistic information from the shape combinations. Moreover, neurons in the parietal cortex reveal the addition and subtraction of probabilistic quantities that underlie decision-making on this task.

Review

The authors argue that the brain reasons probabilistically, because they find that single neuron responses (firing rates) correlate with a measure of probabilistic evidence derived from the probabilistic task setup. It is certainly true that the monkeys could learn the task (a variant of the weather prediction task) and I also find the evidence presented in the paper generally compelling, but the authors note themselves that similar correlations with firing rate may result from other quantitative measures with similar properties as the one considered here. May, for example, firing rates correlate similarly with a measure of expected value of a shape combination as derived from a reinforcement learning model?

What did they do in detail? They trained monkeys on a task in which they had to predict which of two targets will be rewarded based on a set of four shapes presented on the screen. Each shape contributed a certain weight to the probability of rewarding a target as defined by the experimenters. The monkeys had to learn these weights. Then they also had to learn (implicitly) how the weights of shapes are combined to produce the probability of reward. After about 130,000 trials the monkeys were good enough to be tested. The trick in the experiment was that the four shapes were not presented simultaneously, but appeared one after the other. The question was whether neurons in lateral intraparietal (LIP) area of the monkeys’ brains would represent the updated probabilities of reward after addition of each new shape within a trial. That the neurons would do that was hypothesised, because results from previous experiments suggested (see Gold & Shalden, 2007 for review) that neurons in LIP represent accumulated evidence in a perceptual decision making paradigm.

Now Shadlen seems convinced that these neurons do not directly represent the relevant probabilities, but rather represent the log likelihood ratio (logLR) of one choice option over the other (see, e.g., Gold & Shadlen, 2001 and Shadlen et al., 2008). Hence, these ‘posterior’ probabilities play no role in the paper. Instead all results are obtained for the logLR. Funnily the task is defined solely in terms of the posterior probability of reward for a particular combination of four shapes and the logLR needs to be computed from the posterior probabilities (Yang & Shadlen don’t lay out this detail in the paper or the supplementary information). I’m more open about the representation of posterior probabilities directly and I wondered how the correlation with logLR would look like, if the firing rates would respresent posterior probabilities. This is easy to simulate in Matlab (see Yang2007.m). Such a simulation shows that, as a function of logLR, the firing rate (representing posterior probabilities) should follow a sigmoid function. Compare this prediction to Figures 2c and 3b for epoch 4. Such a sigmoidal relationship derives from the boundedness of the posterior probabilities which is obviously reflected in firing rates of neurons as they cannot drop or rise indefinitely. So there could be simple reasons for the boundedness of firing rates other than that they represent probabilities, but in any case it appears unlikely that they represent unbounded log likelihood ratios.

Probabilistic vs. non-probabilistic approaches to the neurobiology of perceptual decision-making.

Drugowitsch, J. and Pouget, A.
Curr Opin Neurobiol, 22:963–969, 2012
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Abstract

Optimal binary perceptual decision making requires accumulation of evidence in the form of a probability distribution that specifies the probability of the choices being correct given the evidence so far. Reward rates can then be maximized by stopping the accumulation when the confidence about either option reaches a threshold. Behavioral and neuronal evidence suggests that humans and animals follow such a probabilitistic decision strategy, although its neural implementation has yet to be fully characterized. Here we show that that diffusion decision models and attractor network models provide an approximation to the optimal strategy only under certain circumstances. In particular, neither model type is sufficiently flexible to encode the reliability of both the momentary and the accumulated evidence, which is a pre-requisite to accumulate evidence of time-varying reliability. Probabilistic population codes, by contrast, can encode these quantities and, as a consequence, have the potential to implement the optimal strategy accurately.

Review

It’s essentially an advertisement for probabilistic population codes (PPCs) for modelling perceptual decisions. In particular, they contrast PPCs to diffusion models and attractor models without going into details. The main argument against attractor models is that they don’t encode a decision confidence in the attractor state. The main argument against diffusion models is that they are not fit to represent varying evidence reliability, but it’s not fully clear to me what they mean by that. The closest I get is that “[…] the drift is a representation of the reliability of the momentary evidence” and they argue that for varying drift rate the diffusion model becomes suboptimal. Of course, if the diffusion model assumes a constant drift rate, it is suboptimal when the drift rate changes, but I’m not sure whether this is the point they are making. The authors mention one potential weak point of PPCs: They predict that the decision bound is defined on a linear combination of integrated momentary evidence, but the firing of neurons in area LIP indicates that the bound is on the estimated correctness of single decisions, i.e., there is a bound for each decision alternative, as in a race model. I interpret this as evidence for a decision model where the bound is defined on the posterior probability of the decision alternatives.

The paper is a bit sloppily written (frequent, easily avoidable language errors).

Representation of confidence associated with a decision by neurons in the parietal cortex.

Kiani, R. and Shadlen, M. N.
Science, 324:759–764, 2009
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Abstract

The degree of confidence in a decision provides a graded and probabilistic assessment of expected outcome. Although neural mechanisms of perceptual decisions have been studied extensively in primates, little is known about the mechanisms underlying choice certainty. We have shown that the same neurons that represent formation of a decision encode certainty about the decision. Rhesus monkeys made decisions about the direction of moving random dots, spanning a range of difficulties. They were rewarded for correct decisions. On some trials, after viewing the stimulus, the monkeys could opt out of the direction decision for a small but certain reward. Monkeys exercised this option in a manner that revealed their degree of certainty. Neurons in parietal cortex represented formation of the direction decision and the degree of certainty underlying the decision to opt out.

Review

The authors used a 2AFC-task with an option to waive the decision in favour of a choice which provides low, but certain reward (the sure option) to investigate the representation of confidence in LIP neurons. Behaviourally the sure option had the expected effect: it was increasingly chosen the harder the decisions were, i.e., the more likely a false response was. Trials in which the sure option was chosen, thus, may be interpreted as those in which the subject was little confident in the upcoming decision. It is important to note that task difficulty here was manipulated by providing limited amounts of information for a limited amount of time, i.e., this was not a reaction time task.

The firing rates of the recorded LIP neurons indicate that selection of the sure option is associated with an intermediate level of activity compared to that of subsequent choices of the actual decision options. For individual trials the authors found that firing rates closer to the mean firing rate (in a short time period before the sure option became available) more frequently lead to selection of the sure option than firing rates further away from the mean, but in absolute terms the activity in this time window could predict choice of the sure option only weakly (probability of 0.4). From these results the authors conclude that the LIP neurons which have previously been found to represent evidence accumulation also encode confidence in a decision. They suggest a simple drift-diffusion model with fixed diffusion parameter to explain the results. Additional to standard diffusion models they define confidence in terms of the log-posterior odds which they compute from the state of the drift-diffusion model. They define posterior as p(S_i|v), the probability that decision option i is correct given that the drift-diffusion state (the decision variable) is v. They compute it from the corresponding likelihood p(v|S_i), but don’t state how they obtained that likelihood. Anyway, the sure option is chosen in the model, when the log-posterior odds is below a certain level. I don’t see why the detour via the log-posterior odds is necessary. You could directly define v as the posterior for decision option i and still be consistent with all the findings in the paper. Of course, then v could not be governed by a linear drift anymore, but why should it in the first place? The authors keenly promote the Bayesian brain, but stop just before the finishing line. Why?

Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks.

Vogels, T. P., Sprekeler, H., Zenke, F., Clopath, C., and Gerstner, W.
Science, 334:1569–1573, 2011
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Abstract

Cortical neurons receive balanced excitatory and inhibitory synaptic currents. Such a balance could be established and maintained in an experience-dependent manner by synaptic plasticity at inhibitory synapses. We show that this mechanism provides an explanation for the sparse firing patterns observed in response to natural stimuli and fits well with a recently observed interaction of excitatory and inhibitory receptive field plasticity. The introduction of inhibitory plasticity in suitable recurrent networks provides a homeostatic mechanism that leads to asynchronous irregular network states. Further, it can accommodate synaptic memories with activity patterns that become indiscernible from the background state but can be reactivated by external stimuli. Our results suggest an essential role of inhibitory plasticity in the formation and maintenance of functional cortical circuitry.

Review

The authors show that, if the same input to an output neuron arrives through an excitatory and a delayed inhibitory channel, synaptic plasticity (a symmetric STDP rule) at the inhibitory synapses leads to “detailed balance”, i.e., to cancellation of excitatory and inhibitory input currents. Then, the output neuron fires sparsely and irregularly (as observed for real neurons) only when an excitatory input was not predicted by the implicit model encoded by the synaptic weights of the inhibitory inputs. The adaptation of the inhibitory synapses also matches potential changes in the excitatory synapses, although here they only present simulations in which excitatory synapses changed abruptly and stayed constant afterwards. (What happens when excitatory and inhibitory synapses change concurrently?) Finally, the authors show that similar results apply to recurrently connected networks of neurons with dedicated inhibitory neurons (balanced networks). Arbitrary activity patterns can be encoded by the excitatory connections, activity in these patterns is then suppressed by the inhibitory neurons, while partial activation of the patterns through external input reactivates the whole patterns (cf. recall of memory) without suppressing potential reactivation of other patterns in the network.

These are interesting ideas, clearly presented and with very detailed supplementary information. The large number of inhibitory neurons in cortex makes the assumed pairing of excitatory and inhibitory input at least possible, but I don’t know how prevalent this really is. Another important assumption here is that the inhibitory input is a bit slower than the excitatory input. This makes intuitive sense, if you assume that the inhibitory input needs to be relayed through an additional inhibitory neuron, but I’ve seen the opposite assumption before, too.

Representational switching by dynamical reorganization of attractor structure in a network model of the prefrontal cortex.

Katori, Y., Sakamoto, K., Saito, N., Tanji, J., Mushiake, H., and Aihara, K.
PLoS Comput Biol, 7:e1002266, 2011
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Abstract

The prefrontal cortex (PFC) plays a crucial role in flexible cognitive behavior by representing task relevant information with its working memory. The working memory with sustained neural activity is described as a neural dynamical system composed of multiple attractors, each attractor of which corresponds to an active state of a cell assembly, representing a fragment of information. Recent studies have revealed that the PFC not only represents multiple sets of information but also switches multiple representations and transforms a set of information to another set depending on a given task context. This representational switching between different sets of information is possibly generated endogenously by flexible network dynamics but details of underlying mechanisms are unclear. Here we propose a dynamically reorganizable attractor network model based on certain internal changes in synaptic connectivity, or short-term plasticity. We construct a network model based on a spiking neuron model with dynamical synapses, which can qualitatively reproduce experimentally demonstrated representational switching in the PFC when a monkey was performing a goal-oriented action-planning task. The model holds multiple sets of information that are required for action planning before and after representational switching by reconfiguration of functional cell assemblies. Furthermore, we analyzed population dynamics of this model with a mean field model and show that the changes in cell assemblies’ configuration correspond to those in attractor structure that can be viewed as a bifurcation process of the dynamical system. This dynamical reorganization of a neural network could be a key to uncovering the mechanism of flexible information processing in the PFC.

Review

Based on firing properties of certain prefrontal cortex neurons the authors suggest a network model in which short-term plasticity implements switches of what the neurons in the network represent. In particular, neurons in prefrontal cortex have been found which switch from representing goals to representing actions (first, their firing varies depending on which goal is shown, then it varies depending on which action is executed afterwards while firing equally for all goals). The authors call this representational switches and they assume that these are implemented via changes in the connection strengths of neurons in a recurrently connected neural network. The network is setup such that network activity always converges to one of several fixed point attractors. A suitable change in connection strengths then leads to a change in the attractor landscape which may be interpreted as a change in what the network represents. The main contribution of the authors is to suggest a particular pattern of short-term plasticity at synapses in the network such that the network exhibits the desired representational switching. Another important aspect of this model is its structure: the network consists of separate cell assemblies, different subsets of which are assumed to be active when either goals or actions are represented and the goal and action subsets are partially overlapping. For example, in their model they have four cell assemblies (A,B,C,D) and the subsets (A,B) and (C,D) are associated with goals while subsets (A,D) and (B,C) are associated with actions. Initially the network is assumed to be in the goal state in which the connection strenghts A-B and C-D are large. The presentation of one of two goals then makes the network activity converge to strong activation of (A,B) or (C,D). Synaptic depression of connections A-B (assuming that this is the active subset) with simultaneous facilitation of connections A-D and B-C then leads to the desired change of connection strengths which implements the representational switch and then makes either subset (A-D), or subset (B-C) the active subset. It is not entirely clear to me why only one action subset becomes active. Maybe this is what the inhibitory units in the model are for (their function is not explained by the authors). In further analysis and experiments the authors confirm the attractor landscape of the model (and how it changes), show that the timing of the representational switch can be influenced by input to the network and show that the probability of changing from a particular goal to a particular action can be manipulated by changing the number of prior connections between the corresponding cell assemblies.

The authors show a nice qualitative correspondence between experimental findings and simulated network behaviour (although some qualitative differences are left, too, e.g., a general increase of firing also for the non-preferred goal and action in the experimental findings). In essence, the authors present a mechanism which could implement the (seemingly) autonomous switching of representations in prefrontal cortex neurons. Whether this mechanism is used by the brain is an entirely different question. I don’t know of evidence backing the chosen special wiring of neurons and distribution of short-term placticity, but this might just reflect my lack of knowledge of the field. Additionally, I wouldn’t exclude the possibility of a hierarchical model. The authors argue against this by presuming that prefrontal cortex already should be the top of the hierarchy, but nothing prevents us to make hierarchical models of prefrontal cortex itself. This points to the mixing of levels of description in the paper: On the one hand, the main contributions of the paper are on the algorithmic level describing the necessary wiring in a network of a few units and how it needs to change to reproduce the behaviour observed in experiments. On the other hand, the main model is on an implementational level showing how these ideas could be implemented in a network of leaky integrate and fire (LIF) neurons. In my opinion, the LIF neuron network doesn’t add anything interesting to the paper apart from the proof that the algorithmic ideas can be implemented by such a network. On the contrary, it masks a bit the main points of the paper by introducing an abundance of additional parameters which needed to be chosen by the authors, but for which we don’t know which of these settings are important. Finally, I wonder how the described network is reset in order to be ready for the next trial. The problem is the following: the authors initialise the network such that the goal subsets have a high synaptic efficacy at the start of the trial. The short-term plasticity then reduces these synaptic efficacies while simultaneously increasing those of the action subsets. At the end of a trial they all end up in a similar range (see Fig. 3A bottom). In order for the network to work as expected in the next trial, it somehow needs to reset to the initial synaptic efficacies.

Probabilistic population codes for Bayesian decision making.

Beck, J. M., Ma, W. J., Kiani, R., Hanks, T., Churchland, A. K., Roitman, J., Shadlen, M. N., Latham, P. E., and Pouget, A.
Neuron, 60:1142–1152, 2008
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Abstract

When making a decision, one must first accumulate evidence, often over time, and then select the appropriate action. Here, we present a neural model of decision making that can perform both evidence accumulation and action selection optimally. More specifically, we show that, given a Poisson-like distribution of spike counts, biological neural networks can accumulate evidence without loss of information through linear integration of neural activity and can select the most likely action through attractor dynamics. This holds for arbitrary correlations, any tuning curves, continuous and discrete variables, and sensory evidence whose reliability varies over time. Our model predicts that the neurons in the lateral intraparietal cortex involved in evidence accumulation encode, on every trial, a probability distribution which predicts the animal’s performance. We present experimental evidence consistent with this prediction and discuss other predictions applicable to more general settings.

Review

In this article the authors apply probabilistic population coding as presented in Ma et al. (2006) to perceptual decision making. In particular, they suggest a hierarchical network with a MT and LIP layer in which the firing rates of MT neurons encode the current evidence for a stimulus while the firing rates of LIP neurons encode the evidence accumulated over time. Under the made assumptions it turns out that the accumulated evidence is independent of nuisance parameters of the stimuli (when they can be interpreted as contrasts) and that LIP neurons only need to sum (integrate) the activity of MT neurons in order to represent the correct posterior of the stimulus given the history of evidence. They also suggest a readout layer implementing a line attractor which reads out the maximum of the posterior under some conditions.

Details

Probabilistic population coding is based on the definition of the likelihood of stimulus features p(r|s,c) as an exponential family distribution of firing rates r. A crucial requirement for the central result of the paper (that LIP only needs to integrate the activity of MT) is that nuisance parameters c of the stimulus s do not occur in the exponential itself while the actual parameters of s only occur in the exponential. This restricts the exponential family distribution to the “Poisson-like family”, as they call it, which requires that the tuning curves of the neurons and their covariance are proportional to the nuisance parameters c (details for this need to be read up in Ma et al., 2006). The point is that this is the case when c corresponds to contrast, or gain, of the stimulus. For the considered random dot stimuli the coherence of the dots may indeed be interpreted as the contrast of the motion in the sense that I can imagine that the tuning curves of the MT neurons are multiplicatively related to the coherence of the dots.

The probabilistic model of the network activities is setup such that the firing of neurons in the network is an indirect, noisy observation of the underlying stimulus, but what we are really interested in is the posterior of the stimulus. So the question is how you can estimate this posterior from the network firing rates. The trick is that under the Poisson-like distribution the likelihood and posterior share the same exponential such that the posterior becomes proportional to this exponential, because the other parts of the likelihood do not depend on the stimulus s (they assume a flat prior of s such that you don’t need to consider it when computing the posterior). Thus, the probability of firing in the network is determined from the likelihood while the resulting firing rates simultaneously encode the posterior. Mind-boggling. The main contribution from the authors then is to show, assuming that firing rates of MT neurons are driven from the stimulus via the corresponding Poisson-like likelihood, that LIP neurons only need to integrate the spikes of MT neurons in order to correctly represent the posterior of the stimulus given all previous evidence (firing of MT neurons). Notice, that they also assume that LIP neurons have the same tuning curves with respect to the stimulus as MT neurons and that the neurons in LIP sum the activity of this MT neuron which they share a tuning curve with. They note that a naive procedure like that, i.e. a single neuron integrating MT firing over time, would quickly saturate its activity. So they show, and that is really cool, that global inhibition in the LIP network does not affect the representation of the posterior, allowing them to prevent saturation of firing while maintaining the probabilistic interpretation.

So far to the theory. In practice, i.e. experiments, the authors do something entirely different, because “these results are important, but they are based on assumptions that are not necessarily exactly true in vivo. […] It is therefore essential that we test our theory in biologically realistic networks.” Now, this is a noble aim, but what exactly do we learn about this theory, if all results are obtained using methods which violate the assumptions of the theory? For example, neither the probability of firing in MT nor LIP is Poisson-like, LIP neurons not just integrate MT activity, but are also recurrently connected, LIP neurons have local inhibition (they are leaky integrators, inhibition between LIP neurons depending on tuning properties) instead of global inhibition and LIP neurons have an otherwise completely unmotivated “urgency signal” whose contribution increases with time (this stems from experimental observations). Without any concrete links between the two models in theory (I guess, the main ideas are similar, but the details are very different) it has to be shown that they are similar using experimental results. In any case, it is hard to differentiate between contributions from the probabilistic theory and the network implementation, i.e., how much of the fit between experimental findings in monkeys and the behaviour of the model is due to the chosen implementation and how much is due to the probabilistic interpretation?

Results

The overall aim of the experiments / simulations in the paper is to show that the proposed probabilistic interpretation is compatible with the experimental findings in monkey LIP. The hypothesis is that LIP neurons encode the posterior of the stimulus as suggested in the theory. This hypothesis is false from the start, because some assumptions of the theory apparently don’t apply to neurons (as acknowledged by the authors). So the new hypothesis is that LIP neurons approximately encode some posterior of the stimulus. The requirement for this posterior is that updates of the posterior should take the uncertainty of the evidence and the uncertainty of the previous estimate of the posterior into account which the authors measure as a linear increase of the log odds of making a correct choice, log[ p(correct) / (1-p(correct)) ], with time together with the dependence of the slope of this linear increase on the coherence (contrast) of the stimulus. I did not follow up why the previous requirement is related to the log odds in this way, but it sounds ok. Remains the question how to estimate the log odds from simulated and real neurons. For the simulated neurons the authors approximate the likelihood with a Poisson-like distribution whose kernel (parameters) were estimated from the simulated firing rates. They argue that it is a good approximation, because linear estimates of the Fisher information appear to be sufficient (I can’t comment on the validity of this argument). A similar approximation of the posterior cannot be done for real LIP neurons, because of a lack of multi-unit recordings which estimate the response of the whole LIP population. Instead, the authors approximate the log odds from measured firing rates of neurons tuned to motion in direction 0 and 180 degrees via a linear regression approach described in the supplemental data.

The authors show that the log-odds computed from the simulated network exhibit the desired properties, i.e., the log-odds linearly increase with time (although there’s a kink at 50ms which supposedly is due to the discretisation) and depend on the coherence of the motion such that the slope of the log-odds increases also when coherence is increased within a trial. The corresponding log-odds of real LIP neurons are far noisier and, thus, do not allow to make definite judgements about linearity. Also, we don’t know whether their slopes would actually change after a change in motion coherence during a trial, as this was never tested (it’s likely, though).

In order to test whether the proposed line attractor network is sufficient to read out the maximum of the posterior in all conditions (readout time and motion coherence) the authors compare a single (global) readout with local readouts adapted for a particular pair of readout time and motion coherence. However, the authors don’t actually use attractor networks in these experiments, but note that these are equivalent to local linear estimators and so use these. Instead of comparing the readouts from these estimators with the actual maximum of the posterior, they only compare the variance of the estimators (Fisher information) which they show to be roughly the same for the local and global estimators. From this they conclude that a single, global attractor network could read out the maximum of the (approximated) posterior. However, this is only true, if there’s no additional bias of the global estimator which we cannot see from these results.

In an additional analysis the authors show that the model qualitatively replicates the behavioural variables (probability correct and reaction time). However, these are determined from the LIP activities in a surprisingly ad-hoc way: the decision time is determined as the time when any one of the simulated LIP neurons reaches a threshold defined on the probability of firing and the decision is determined as the preferred direction of the neuron hitting the threshold (for 2 and 4 choice tasks the response is determined as the quadrant of the motion direction in which the preferred direction of the neuron falls). Why do the authors not use the attractor network to readout the response here? Also, the authors use a lower threshold for the 4-choice task than for the 2-choice task. This is strange, because one of the main findings of the Churchland et al. (2008) paper was that the decision in both, 2- and 4-choice tasks, appears to be determined by a common decision threshold while the initial firing rates of LIP neurons were lower for 4-choice tasks. Here, they also initialise with lower firing rates in the 4-choice task, but additionally choose a lower threshold. They don’t motivate this. Maybe it was necessary to fit the data from Churchland et al. (2008). This discrepancy between data and model is even more striking as the authors of the two papers partially overlap. So, do they deem the corresponding findings of Churchland et al. (2008) not important enough to be modelled, is it impossible to be modelled within their framework, or did they simply forget?

Finally, also the build-up rates of LIP neurons seem to be qualitatively similar in the simulation and the data, although they are consistently lower in the model. The build-up rates for the model are estimated from the first 50ms within each trial. However, the log-odds ratio had this kink at 50ms after which its slope was larger. So, if this effect is also seen directly in the firing rates, the fit of the build-up rates to the data may even be better, if probability of firing after 50ms is used. In Fig. 2C no such kink can be seen in the firing rates, but this is only data for 2 neurons in the model.

Conclusion

Overall the paper is very interesting and stimulating. It is well written and full of sound theoretical results which originate from previous work of the authors. Unfortunately, biological nature does not completely fit the beautiful theory. Consequently, the authors run experiments with more plausible neural networks which only approximately implement the theory. So what conclusions can we draw from the presented results? As long as the firing of MT neurons reflects the likelihood of a stimulus (their MT network is setup in this way), probably a wide range of networks which accumulate this firing will show responses similar to real LIP neurons. It is not easy to say whether this is a consequence of the theory, which states that MT firing rates should be simply summed over time in order to get the right posterior, because of the violation of the assumptions of the theory in more realistic networks. It could also be that more complicated forms of accumulation are necessary such that LIP firing represents the correct posterior. Simple summing then just represents a simple approximation. Also, I don’t believe that the presented results can rule out the possibility of sampling based coding of probabilities (see Fiser et al., 2010) for decision making as long as also the sampling approach would implement some kind of accumulation procedure (think of particle filters – the implementation in a recurrent neural network would probably be quite similar).

Nevertheless, the main point of the paper is that the activity in LIP represents the full posterior and not only MAP estimates or log-odds. Consequently, the model very easily extends to the case of continuous directions of motion which is in contrast to previous, e.g., attractor-based, neural models. I like this idea. However, I cannot determine from the experiments whether their network actually implements the correct posterior, because all their tests yield only indirect measures based on approximated analyses. Even so, it is pretty much impossible to verify that the firing of LIP neurons fits to the simulated results as long as we cannot measure firing of a large part of the corresponding neural population in LIP.